Abstract

The concentration of oxygen in the brain spontaneously fluctuates, and the distribution of power in these fluctuations has a 1/f-like spectra, where the power present at low frequencies of the power spectrum is orders of magnitude higher than at higher frequencies. Though these oscillations have been interpreted as being driven by neural activity, the origin of these 1/f-like oscillations is not well understood. Here, to gain insight of the origin of the 1/f-like oxygen fluctuations, we investigated the dynamics of tissue oxygenation and neural activity in awake behaving mice. We found that oxygen signal recorded from the cortex of mice had 1/f-like spectra. However, band-limited power in the local field potential did not show corresponding 1/f-like fluctuations. When local neural activity was suppressed, the 1/f-like fluctuations in oxygen concentration persisted. Two-photon measurements of erythrocyte spacing fluctuations and mathematical modeling show that stochastic fluctuations in erythrocyte flow could underlie 1/f-like dynamics in oxygenation. These results suggest that the discrete nature of erythrocytes and their irregular flow, rather than fluctuations in neural activity, could drive 1/f-like fluctuations in tissue oxygenation.

Highlights

  • Fluctuations in oxygen tension are ubiquitous throughout the body and are found in muscle tissue and tumors [1], in the retina [2,3], in the carotid artery [4], and in the cortex [5,6,7,8,9,10,11,12]

  • 9 mice were used to measure red blood cell (RBC) spacing in capillaries using two-photon laser scanning microscopy (2PLSM)

  • While we found that the majority of the observed oxygen fluctuations could not be explained by neural activity (Figs 3 and 4), if the relationship between neural activity and oxygenation is not captured by the hemodynamic response function (HRF), such as the nonlinearity of brain hemodynamics [141], some aspect of neural activity might still explain the oxygen fluctuations

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Summary

Introduction

Fluctuations in oxygen tension are ubiquitous throughout the body and are found in muscle tissue and tumors [1], in the retina [2,3], in the carotid artery [4], and in the cortex [5,6,7,8,9,10,11,12]. Despite their ubiquity, relatively little is understood about the origin of these oxygen fluctuations. The hallmark of 1/f-like signals is that the power at lower frequencies is much larger than at higher

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