Locally induced neuronal synchrony precisely propagates to specific cortical areas without rhythm distortion

Propagation of oscillatory spike firing activity at specific frequencies plays an important role in distributed cortical networks. However, there is limited evidence for how such frequency-specific signals are induced or how the signal spectra of the propagating signals are modulated during across-layer (radial) and inter-areal (tangential) neuronal interactions. To directly evaluate the direction specificity of spectral changes in a spiking cortical network, we selectively photostimulated infragranular excitatory neurons in the rat primary visual cortex (V1) at a supra-threshold level with various frequencies, and recorded local field potentials (LFPs) at the infragranular stimulation site, the cortical surface site immediately above the stimulation site in V1, and cortical surface sites outside V1. We found a significant reduction of LFP powers during radial propagation, especially at high-frequency stimulation conditions. Moreover, low-gamma-band dominant rhythms were transiently induced during radial propagation. Contrastingly, inter-areal LFP propagation, directed to specific cortical sites, accompanied no significant signal reduction nor gamma-band power induction. We propose an anisotropic mechanism for signal processing in the spiking cortical network, in which the neuronal rhythms are locally induced/modulated along the radial direction, and then propagate without distortion via intrinsic horizontal connections for spatiotemporally precise, inter-areal communication.

[1]  A. Nambu,et al.  Disruption of actin‐binding domain‐containing Dystonin protein causes dystonia musculorum in mice , 2014, The European journal of neuroscience.

[2]  Takafumi Suzuki,et al.  Simultaneous recording of ECoG and intracortical neuronal activity using a flexible multichannel electrode-mesh in visual cortex , 2011, NeuroImage.

[3]  Y. Isomura,et al.  In Vivo Spiking Dynamics of Intra- and Extratelencephalic Projection Neurons in Rat Motor Cortex , 2018, Cerebral cortex.

[4]  Demetris K. Roumis,et al.  Functional Specialization of Mouse Higher Visual Cortical Areas , 2011, Neuron.

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

[6]  B. Connors,et al.  Electrophysiological and morphological properties of neurons in layer 5 of the rat postrhinal cortex , 2012, Hippocampus.

[7]  Karl Deisseroth,et al.  Recent advances in optogenetics and pharmacogenetics , 2013, Brain Research.

[8]  S. Luck,et al.  The effects of electrode impedance on data quality and statistical significance in ERP recordings. , 2010, Psychophysiology.

[9]  C. Koch,et al.  The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes , 2012, Nature Reviews Neuroscience.

[10]  K. Deisseroth,et al.  Ultrafast optogenetic control , 2010, Nature Neuroscience.

[11]  K. Mabuchi,et al.  Parylene flexible neural probes integrated with microfluidic channels. , 2005, Lab on a chip.

[12]  Kevin W. Kelley,et al.  Astrocytes: The Final Frontier… , 2016, Neuron.

[13]  Heikki Tanila,et al.  Vision in laboratory rodents—Tools to measure it and implications for behavioral research , 2017, Behavioural Brain Research.

[14]  Maria V. Sanchez-Vives,et al.  Electrophysiological classes of cat primary visual cortical neurons in vivo as revealed by quantitative analyses. , 2003, Journal of neurophysiology.

[15]  Jing Wang,et al.  Integrated device for combined optical neuromodulation and electrical recording for chronic in vivo applications , 2012, Journal of neural engineering.

[16]  Jing Wang,et al.  A coaxial optrode as multifunction write-read probe for optogenetic studies in non-human primates , 2013, Journal of Neuroscience Methods.

[17]  Edward M. Callaway,et al.  Feedforward, feedback and inhibitory connections in primate visual cortex , 2004, Neural Networks.

[18]  Claude Bédard,et al.  Generalized cable theory for neurons in complex and heterogeneous media. , 2013, Physical review. E, Statistical, nonlinear, and soft matter physics.

[19]  H. Kennedy,et al.  Alpha-Beta and Gamma Rhythms Subserve Feedback and Feedforward Influences among Human Visual Cortical Areas , 2016, Neuron.

[20]  K. Deisseroth,et al.  Parvalbumin neurons and gamma rhythms enhance cortical circuit performance , 2009, Nature.

[21]  Kenji F. Tanaka,et al.  Identification of Optogenetically Activated Striatal Medium Spiny Neurons by Npas4 Expression , 2012, PloS one.

[22]  U. Knoblich,et al.  Optogenetic drive of neocortical pyramidal neurons generates fMRI signals that are correlated with spiking activity , 2013, Brain Research.

[23]  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.

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

[25]  Anne-Lise Giraud,et al.  The contribution of frequency-specific activity to hierarchical information processing in the human auditory cortex , 2014, Nature Communications.

[26]  Lief E. Fenno,et al.  Principles for applying optogenetic tools derived from direct comparative analysis of microbial opsins , 2011, Nature Methods.

[27]  James B. Aimone,et al.  N2A: a computational tool for modeling from neurons to algorithms , 2014, Front. Neural Circuits.

[28]  H. Takebayashi,et al.  Regional- and temporal-dependent changes in the differentiation of Olig2 progenitors in the forebrain, and the impact on astrocyte development in the dorsal pallium. , 2008, Developmental biology.

[29]  G. Marko‐Varga,et al.  Hypoxia regulates global membrane protein endocytosis through caveolin-1 in cancer cells , 2016, Nature Communications.

[30]  Matthew J Nelson,et al.  Do electrode properties create a problem in interpreting local field potential recordings? , 2010, Journal of neurophysiology.

[31]  K. Mabuchi,et al.  Flexible neural probes with micro-fluidic channels for stable interface with the nervous system , 2004, The 26th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[32]  B. Litt,et al.  High-frequency oscillations in human temporal lobe: simultaneous microwire and clinical macroelectrode recordings. , 2008, Brain : a journal of neurology.

[33]  K. Deisseroth,et al.  Millisecond-timescale, genetically targeted optical control of neural activity , 2005, Nature Neuroscience.

[34]  Y. Kamitani,et al.  Associative-memory representations emerge as shared spatial patterns of theta activity spanning the primate temporal cortex , 2016, Nature Communications.

[35]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[36]  T. Ishizuka,et al.  Optogenetic manipulation of neural and non‐neural functions , 2013, Development, growth & differentiation.

[37]  Raag D. Airan,et al.  Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures , 2010, Nature Protocols.

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

[39]  Jacob G. Bernstein,et al.  Millisecond-Timescale Optical Control of Neural Dynamics in the Nonhuman Primate Brain , 2009, Neuron.

[40]  R. Buckner,et al.  Mapping brain networks in awake mice using combined optical neural control and fMRI. , 2011, Journal of neurophysiology.

[41]  D. Tampellini,et al.  Synaptic activity and Alzheimer's disease: a critical update , 2015, Front. Neurosci..

[42]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[43]  Douglas J. Bakkum,et al.  Revealing neuronal function through microelectrode array recordings , 2015, Front. Neurosci..

[44]  K. Harris,et al.  Cortical connectivity and sensory coding , 2013, Nature.

[45]  Claude Bédard,et al.  A modified cable formalism for modeling neuronal membranes at high frequencies. , 2007, Biophysical journal.

[46]  Jessica A. Cardin,et al.  Stimulus Feature Selectivity in Excitatory and Inhibitory Neurons in Primary Visual Cortex , 2007, The Journal of Neuroscience.

[47]  B. J. Clark,et al.  Cortical connectivity maps reveal anatomically distinct areas in the parietal cortex of the rat , 2015, Front. Neural Circuits.

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

[49]  A. Thomson,et al.  Interlaminar connections in the neocortex. , 2003, Cerebral cortex.

[50]  K. Deisseroth,et al.  High-efficiency channelrhodopsins for fast neuronal stimulation at low light levels , 2011, Proceedings of the National Academy of Sciences.

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

[52]  N. Logothetis,et al.  In Vivo Measurement of Cortical Impedance Spectrum in Monkeys: Implications for Signal Propagation , 2007, Neuron.

[53]  Jin Hyung Lee,et al.  Informing brain connectivity with optogenetic functional magnetic resonance imaging , 2012, NeuroImage.

[54]  K. Nakahara,et al.  Intrasulcal Electrocorticography in Macaque Monkeys with Minimally Invasive Neurosurgical Protocols , 2011, Front. Syst. Neurosci..

[55]  T. Sejnowski,et al.  Dynamic Brain Sources of Visual Evoked Responses , 2002, Science.

[56]  Hiroyuki Ohsaki,et al.  Opto-fMRI analysis for exploring the neuronal connectivity of the hippocampal formation in rats , 2012, Neuroscience Research.

[57]  K. Nakahara,et al.  Local and retrograde gene transfer into primate neuronal pathways via adeno-associated virus serotype 8 and 9 , 2011, Neuroscience.