Coupling of Low Frequency Hemodynamic Oscillations between the Brain and Spinal Cord

Poster No:

2617 

Submission Type:

Abstract Submission 

Authors:

Andrew John Frels1, Vidhya Vijayakrishnan Nair1, Yunjie Tong1

Institutions:

1Purdue University, West Lafayette, IN

First Author:

Andrew John Frels  
Purdue University
West Lafayette, IN

Co-Author(s):

Vidhya Vijayakrishnan Nair  
Purdue University
West Lafayette, IN
Yunjie Tong  
Purdue University
West Lafayette, IN

Introduction:

In functional Magnetic Resonance Imaging (fMRI), the primary contrast is Blood Oxygen Level Dependent (BOLD) signal. It is widely used as a signal of neuronal activity as it tracks increases and decreases in regional blood flow due to neurovascular coupling. Hemodynamic Low Frequency Oscillations (LFO) are BOLD fMRI signals between 0.01 Hz and 0.1 Hz that have been shown to strongly couple to neuronal activation and systemic physiological processes[1]. Delay times between LFOs are consistent with blood arrival and can be used to track cerebral circulation[2,3]. The Central Nervous System (CNS) is comprised of the brain and spinal cord (SC). The presence of LFO signals in the brain is well documented but LFOs as physiological oscillations in the SC have not been investigated; they have only been used to examine direct SC neuronal activity, not brain-SC interactivity[4,5]. There is no evidence on how physiological SC-LFOs couple to brain LFOs. Thus, the primary goal of this study is to investigate the coupling between brain and SC physiological LFO signals across time and frequency. This coupling information could inform a new marker for vascular connectivity between in the CNS. This is important from the perspective of CNS cerebrospinal fluid movement as hemodynamic LFOs have been shown to drive CSF motion in the brain[4]. Future studies could then understand the pathophysiology of traumatic brain or SC injury related degradation of glymphatic clearance.

Methods:

All MRI data were acquired using a 3T SIEMENS MRI scanner with a 64-channel head coil, including structural T1-weighted MPRAGE and fMRI. Data from 11 participants were included in the analysis. The fMRI data were preprocessed using the FMRIB Software Library[6]. To obtain the global mean signal the high-res (T1w) brain mask was registered to the processed fMRI space and the time series was extracted[3]. All fMRI scans had arching in the cervical spine due to magnetic phenomena from distortions caused by bone/tissue interfaces[7] preventing conventional registration of SC masks from T1w space to fMRI space. Instead, the SC was masked in the fMRI space using an in-house algorithm. The SC was defined from the bottom of the scan to the voxel below the cerebellum to ensure inter-subject repeatability; time series were then directly extracted. To assess coupling between the SC and brain in the LFO range, maximum cross-correlation coefficients (MCCC) and delay times were calculated between SC and brain LFOs. For frequency analyses, the power spectra of the SC and brain time series were studied and cross spectral analyses were performed to examine the overlap in frequency content between the signals.
Supporting Image: Figure1.png
   ·Figure 1. Methodology and Time Series Example
 

Results:

Significant MCCCs are found between brain and SC time series in the LFO range indicating meaningful delays. These delays fall into two categories: a negative delay indicates the brain leads the SC while a positive delay shows the SC leads the brain (Fig. 2a-c). Seven subjects have a negative delay (mean=-3.86s) and a positive MCCC while four have a positive delay (mean=4.69s) and a negative MCCC. Variances are hypothesized to originate from the differing lengths of arterial pathways to the brain and SC between subjects. In the frequency analysis (Fig. 2d,e) it can be seen that LFO signals are dominant in the SC and brain. There exists a clear overlap in frequency between the brain and SC, with the highest power in the LFO range.
Supporting Image: Figure2.png
   ·Figure 2. Results showing plot of MCCC vs Delay and example group Time Series and Power Spectra
 

Conclusions:

Our research demonstrates a robust correlation between brain activity and SC-LFOs in both temporal and spectral domains. This investigation is the first study to confirm a significant physiological interconnection between brain and SC LFOs in healthy adult subjects. The findings of this study provide a critical basis for future explorations into spinal cord injuries. In subsequent studies, fMRI can be employed to assess and monitor hemodynamic coherence between the brain and SC, thereby facilitating the evaluation of recovery processes.

Neuroanatomy, Physiology, Metabolism and Neurotransmission:

Anatomy and Functional Systems
Neuroanatomy Other

Novel Imaging Acquisition Methods:

BOLD fMRI 2

Physiology, Metabolism and Neurotransmission :

Neurophysiology of Imaging Signals 1
Physiology, Metabolism and Neurotransmission Other

Keywords:

Cerebral Blood Flow
FUNCTIONAL MRI
Spinal Cord

1|2Indicates the priority used for review

Provide references using author date format

1. Tong, Y. & Frederick, B. de B. Time lag dependent multimodal processing of concurrent fMRI and near-infrared spectroscopy (NIRS) data suggests a global circulatory origin for low-frequency oscillation signals in human brain. Neuroimage 53, 553–564 (2010).
2. Tong, Y., Yao, J. (Fiona), Chen, J. J. & Frederick, B. de B. The resting-state fMRI arterial signal predicts differential blood transit time through the brain. Journal of Cerebral Blood Flow and Metabolism 39, 1148–1160 (2019).
3. Yao, J. et al. Cerebral circulation time derived from fMRI signals in large blood vessels. Journal of Magnetic Resonance Imaging 50, 1504–1513 (2019).
4. Barry, R. L., Vannesjo, S. J., By, S., Gore, J. C. & Smith, S. A. Spinal cord MRI at 7T. Neuroimage 168, 437–451 (2018).
5. Yang, H. C. et al. Coupling between cerebrovascular oscillations and CSF flow fluctuations during wakefulness: An fMRI study. Journal of Cerebral Blood Flow & Metabolism 42, 1091 (2022).
6. Jenkinson, M., Beckmann, C. F., Behrens, T. E. J., Woolrich, M. W. & Smith, S. M. FSL. Neuroimage 62, 782–790 (2012).
7. Stroman, P. W. et al. The current state-of-the-art of spinal cord imaging: Methods. Neuroimage 84, 1070–1081 (2014).