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

Haruo Toda,Asim K Bepari,Takafumi Suzuki,Sho Sato,Masao Horie,Isao Hasegawa,Kiyoshi Nakahara,Hirohito Sawahata,Hirohide Takebayashi,Haruo Okado,Keisuke Kawasaki

doi:10.1038/s41598-018-26054-8

Haruo Toda, Asim K Bepari + Show 9 more

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https://doi.org/10.1038/s41598-018-26054-8

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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.

Highlights

Propagation of oscillatory spike firing activity with specific frequencies plays important roles in large-scale cortical networks[1,2,3,4,5]
We developed a new combination of optogenetics and micro-electrocorticogram[11] for simultaneous characterization of radial and tangential cortical propagation with oscillatory spike activity
Spectral changes during radial local field potentials (LFPs) propagation can be estimated by comparing the signals at V1deep and V1surf, while those during tangential signal propagation can be estimated by comparing signals at Ex-V1 and V1surf

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Propagation of oscillatory spike firing activity with specific frequencies plays important roles in large-scale cortical networks[1,2,3,4,5]. Radial- and tangential spectral change (frequency-specific reduction or induction of the neuronal spike rhythm) are simultaneously evaluated within the same tissue. It should be noted here that the tangential signal propagation must be non-linear presumably due to anisotropy of anatomical connectivity, physiological validation of this view has been difficult due to the lack of appropriate methods to regularly sample oscillatory neural activity from a wide area of active cortical circuits. This is why many previous studies employed subthreshold stimulation and regarded the brain tissue as a volume conductor. Our analyses focused on two classes of frequency components: the responses at the stimulation frequencies, and non-stimulation components which was not included in the stimulation frequencies or their harmonics

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