Identifying Anatomical Origins of Coexisting Oscillations in the Cortical Microcircuit

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-γ 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-γ peak turns out to be generated in a sub-circuit located in layer 2/3 and 4, while the high-γ 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.Author Summary: Recordings of brain activity show multiple coexisting oscillations. The generation of these oscillations has so far only been investigated in generic one- and two-population networks, neglecting their embedment into larger systems. We introduce a method that determines the mechanisms and sub-circuits generating oscillations in structured spiking networks. Analyzing a multi-layered model of the cortical microcircuit, we trace back characteristic oscillations to experimentally observed connectivity patterns. The approach exposes the influence of individual connections on frequency and amplitude of these oscillations and therefore reveals locations, where biological mechanisms controlling oscillations and experimental manipulations have the largest impact. The new analytical tool replaces parameter scans in computationally expensive models, guides circuit design, and can be employed to validate connectivity data.