Cortex-wide neuronal dynamics underpin quasi-periodic patterns in resting-state fMRI

Functional magnetic resonance imaging (fMRI) captures whole-brain activity fluctuations non-invasively in humans and animals. Beyond task/stimuli-locked responses, fMRI measures large-scale patterned activity during rest. Among these, quasi-periodic patterns (QPPs) represent recurring waves of activity that unfold over seconds and exhibit consistent spatiotemporal characteristics.

Notably, certain fMRI-QPPs are well-preserved across species and altered in various neuropsychiatric and neurodegenerative diseases. Yet, our collective understanding of their neural underpinnings is limited given the indirect nature of the blood-oxygen-level-dependent (BOLD) fMRI signal. Simultaneous measures of local field potentials have provided some affirmation that fMRI-QPPs have neural origins, but these point-measurements are limited to a handful of sites.

Here, we use a unique multimodal implementation of simultaneous wide-field calcium (WF-Ca2+) imaging and fMRI to investigate the neural origins of fMRI-based QPPs. We uncover a robust time-locked correlation between QPPs detected by cortex-wide fluorescent WF-Ca2+ imaging of neural activity and QPPs of BOLD-fMRI. These data validate the hypothesis that BOLD-fMRI QPPs derive from preceding slow waves of neural activity with regional and temporal precision.

Joel Greenwood, Paul Shamble, and Omer Mano from Neurotechnology Core of the Kavli Institute for Neuroscience at Yale and the team members of the Magnetic Resonance Research Center at Yale University for their technological expertise. Joanes Grandjean for critical discussion. Yonghyun Ha and Chenhao Sun for hardware support.

Crair for experimental expertise. C.H. was supported by NIH R25MH119043. E.M.R.L., F.M., S.M.S. were supported by NIH R01 NS130069-01.

S.M.S. was supported by P30AG066508. Department of Radiology and Biomedical Imaging, Yale School of Medicine, New Haven, CT, USA Francesca Mandino, Xilin Shen, Xenophon Papademetris & Evelyn M. Lake Yale Biomedical Imaging Institute, Yale University, New Haven, CT, USA Department of Psychiatry, University of Pennsylvania, Philadelphia, PA, USA Department of Biomedical Engineering, Yale University, New Haven, CT, USA Xenophon Papademetris & Evelyn M.