Identifying anatomical origins of coexisting oscillations in the cortical microcircuit

TL;DR

This study develops a systematic theoretical approach to identify the specific anatomical circuits responsible for generating different oscillation frequencies in cortical microcircuits, combining modeling, analysis, and sensitivity measures.

Contribution

It introduces a novel method to pinpoint the neural connections underlying oscillations, revealing the minimal circuits responsible for low- and high-gamma activity.

Findings

Low-gamma oscillations originate in layer 2/3 and 4 sub-circuits.

High-gamma oscillations emerge from layer 4 interneurons.

Perturbations to key connections significantly alter spectral properties.

Abstract

Oscillations are omnipresent in neural population signals, like multi-unit recordings, EEG/MEG, and the local field potential. They have been linked to the population firing rate of neurons, with individual neurons firing in a close-to-irregular fashion at low rates. Using a combination of mean-field and linear response theory we predict the spectra generated in a layered microcircuit model of V1, composed of leaky integrate-and-fire neurons and based on connectivity compiled from anatomical and electrophysiological studies. The model exhibits low- and high-gamma oscillations visible in all populations. Since locally generated frequencies are imposed onto other populations, the origin of the oscillations cannot be deduced from the spectra. We develop an universally applicable systematic approach that identifies the anatomical circuits underlying the generation of oscillations in a given network. Based on a theoretical reduction of the dynamics, we derive a sensitivity measure resulting in a frequency-dependent connectivity map that reveals connections crucial for the peak amplitude and frequency of the observed oscillations and identifies the minimal circuit generating a given frequency. The low-gamma peak turns out to be generated in a sub-circuit located in layer 2/3 and 4, while the high-gamma peak emerges from the inter-neurons in layer 4. Connections within and onto layer 5 are found to regulate slow rate fluctuations. We further demonstrate how small perturbations of the crucial connections have significant impact on the population spectra, while the impairment of other connections leaves the dynamics on the population level unaltered. The study uncovers connections where mechanisms controlling the spectra of the cortical microcircuit are most effective.