Respiratory-related brain pulsations are increased in epilepsy-a two-centre functional MRI study

Janne Kananen; Heta Helakari; Vesa Korhonen; Niko Huotari; Matti Järvelä; Lauri Raitamaa; Ville Raatikainen; Zalan Rajna; Timo Tuovinen; Maiken Nedergaard; Julia Jacobs; Pierre LeVan; Hanna Ansakorpi; Vesa Kiviniemi

doi:10.1093/braincomms/fcaa076

Respiratory-related brain pulsations are increased in epilepsy-a two-centre functional MRI study

Brain Commun. 2020 Jun 8;2(2):fcaa076. doi: 10.1093/braincomms/fcaa076. eCollection 2020.

Authors

Janne Kananen^{1

2

3}, Heta Helakari^{1

2

3}, Vesa Korhonen^{1

2

3}, Niko Huotari^{1

2

3}, Matti Järvelä^{1

2

3}, Lauri Raitamaa^{1

2

3}, Ville Raatikainen^{1

2

3}, Zalan Rajna^{1

4}, Timo Tuovinen^{1

2

3}, Maiken Nedergaard^{5

6}, Julia Jacobs^{7

8

9

10}, Pierre LeVan^{8

9

10

11

12}, Hanna Ansakorpi^{3

13

14}, Vesa Kiviniemi^{1

2

3}

Affiliations

¹ Oulu Functional NeuroImaging (OFNI), Department of Diagnostic Radiology, Oulu University Hospital, Oulu 90029, Finland.
² Medical Imaging, Physics and Technology (MIPT), Faculty of Medicine, University of Oulu, Oulu 90220, Finland.
³ Medical Research Center (MRC), Oulu 90220, Finland.
⁴ Center for Machine Vision and Signal Analysis (CMVS), University of Oulu, Oulu 90014, Finland.
⁵ Center for Translational Neuromedicine, Department of Neurosurgery, University of Rochester Medical Center, Rochester, NY 14642, USA.
⁶ Center for Translational Neuromedicine, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen 2200, Denmark.
⁷ Department of Pediatric Neurology and Muscular Disease, University Medical Center Freiburg, Faculty of Medicine, University of Freiburg, Freiburg 79110, Germany.
⁸ Department of Paediatrics, Cumming School of Medicine, University of Calgary, Calgary, AB T2N 4N1, Canada.
⁹ Department of Neuroscience, Cumming School of Medicine, University of Calgary, Calgary, AB T2N 4N1, Canada.
¹⁰ Hotchkiss Brain Institute and Alberta Children's Hospital Research Institute, University of Calgary, Calgary, AB T2N 4N1, Canada.
¹¹ Department of Radiology, Medical Physics, University Medical Center Freiburg, Faculty of Medicine, University of Freiburg, Freiburg 79110, Germany.
¹² Department of Radiology, Cumming School of Medicine, University of Calgary, Calgary, AB T2N 4N1, Canada.
¹³ Research Unit of Neuroscience, Neurology, University of Oulu, Oulu 90220, Finland.
¹⁴ Department of Neurology, Oulu University Hospital, Oulu 90029, Finland.

Abstract

Resting-state functional MRI has shown potential for detecting changes in cerebral blood oxygen level-dependent signal in patients with epilepsy, even in the absence of epileptiform activity. Furthermore, it has been suggested that coefficient of variation mapping of fast functional MRI signal may provide a powerful tool for the identification of intrinsic brain pulsations in neurological diseases such as dementia, stroke and epilepsy. In this study, we used fast functional MRI sequence (magnetic resonance encephalography) to acquire ten whole-brain images per second. We used the functional MRI data to compare physiological brain pulsations between healthy controls (n = 102) and patients with epilepsy (n = 33) and furthermore to drug-naive seizure patients (n = 9). Analyses were performed by calculating coefficient of variation and spectral power in full band and filtered sub-bands. Brain pulsations in the respiratory-related frequency sub-band (0.11-0.51 Hz) were significantly (P < 0.05) increased in patients with epilepsy, with an increase in both signal variance and power. At the individual level, over 80% of medicated and drug-naive seizure patients exhibited areas of abnormal brain signal power that correlated well with the known clinical diagnosis, while none of the controls showed signs of abnormality with the same threshold. The differences were most apparent in the basal brain structures, respiratory centres of brain stem, midbrain and temporal lobes. Notably, full-band, very low frequency (0.01-0.1 Hz) and cardiovascular (0.8-1.76 Hz) brain pulses showed no differences between groups. This study extends and confirms our previous results of abnormal fast functional MRI signal variance in epilepsy patients. Only respiratory-related brain pulsations were clearly increased with no changes in either physiological cardiorespiratory rates or head motion between the subjects. The regional alterations in brain pulsations suggest that mechanisms driving the cerebrospinal fluid homeostasis may be altered in epilepsy. Magnetic resonance encephalography has both increased sensitivity and high specificity for detecting the increased brain pulsations, particularly in times when other tools for locating epileptogenic areas remain inconclusive.

Keywords: brain physiology; brain pulsations; epilepsy; fast fMRI; respiration.

Grants and funding

R01 NS100366/NS/NINDS NIH HHS/United States