In vivo direct imaging of neuronal activity at high temporospatial resolution

Abstract

There has been a long-standing demand for noninvasive neuroimaging methods that can detect neuronal activity at both high temporal and high spatial resolution. We present a two-dimensional fast line-scan approach that enables direct imaging of neuronal activity with millisecond precision while retaining the high spatial resolution of magnetic resonance imaging (MRI). This approach was demonstrated through in vivo mouse brain imaging at 9.4 tesla during electrical whisker-pad stimulation. In vivo spike recording and optogenetics confirmed the high correlation of the observed MRI signal with neural activity. It also captured the sequential and laminar-specific propagation of neuronal activity along the thalamocortical pathway. This high-resolution, direct imaging of neuronal activity will open up new avenues in brain science by providing a deeper understanding of the brain’s functional organization, including the temporospatial dynamics of neural networks.

Intrinsic macroscale oscillatory modes driving long range functional connectivity detected with ultrafast fMRI

“…Recent studies combining simultaneous electrophysiological recordings of local field potentials (LFPs) and fMRI in rats reported significant coherence between the two signals precisely in the range of frequencies detected herein (Pan, Thompson et al 2013, Thompson, Pan et al 2014). Therefore, one cannot exclude the possibility that the oscillations observed with fMRI are linked with other factors beyond blood flow/volume effects alone, and may provide a more direct measurement of neuronal activity (Lewis, Setsompop et al 2016, Toi, Jang et al 2022). Still, given that hemodynamic blurring is expected (Gonzalez-Castillo, J., Saad, Z.S., et al, 2012.)…”

“…While previous ultrafast fMRI experiments in rodents have reached up to 20 frames per second, they have focused mostly on stimulus-driven responses in specific regions of interest (Yu, Qian et al 2014, Yu, He et al 2016, Kay, Jamison et al 2020, Lake, Ge et al 2020, Gil, Fernandes et al 2021), and much remains to be explored at the level of spontaneous long-range interactions. Allowing for a large span of scales both in space (from micrometer to meter) and in time (from millisecond to hour), exploring the full possibilities of MRI may provide relevant insights into the brain organizational principles in the spatial, temporal, and spectral domains (Toi, Jang et al 2022). Indeed, the traditionally low temporal resolution of fMRI studies has limited the analysis to spatial correlations between ultra-slow fluctuations in distant areas.…”

“…) (Yu, Qian et al 2014, Yu, He et al 2016, Kay, Jamison et al 2020, Lake, Ge et al 2020, Gil, Fernandes et al 2021, and much remains to be explored at the level of spontaneous long-range interactions. Allowing for a large span of scales both in space (from micrometer to meter) and in time (from millisecond to hour), exploring the full possibilities of MRI may provide relevant insights into the brain organizational principles in the spatial, temporal, and spectral domains (Toi, Jang et al 2022).…”

Cortical networks relating to arousal are differentially coupled to neural activity and hemodynamics

“…Band-limited LFP is known to correlate to BOLD, but infraslow LFP waves have also been shown to be compatible in time scale with the slow BOLD fluctuations that occur in spontaneous activity making them ideal candidates for the neural basis of the BOLD signal and for coordinating activity between large-scale brain regions (Pan, Thompson, Magnuson, Jaeger, & Keilholz, 2013). Neuroimaging advances measuring in vivo at both high temporal and spatial resolution hold a lot of promise for probing this relationship across different scales (Lewis, Setsompop, Rosen, & Polimeni, 2016; Toi et al, 2022).…”

Ultra-high field neuroimaging in psychosis: A narrative review

“…Moreover, UHF confers increased temporal resolution as well as shortened acquisition times in some cases, which allows for greater sensitivity and benefits participants with less time in the scanner, which is particularly relevant for those with psychiatric disorders, such as schizophrenia. Novel techniques, including direct imaging of neuronal activity (DIANA-fMRI) recently demonstrated in rodents ( 52 ), offer unprecedented potential to combine spatial and temporal resolution to make precise neurophysiological inferences using UHF-fMRI.…”