Neural Dynamics during Resting State: A Functional Magnetic Resonance Imaging Exploration with Reduction and Visualization

The brain is a complex high-order system. Body movements or mental activities are both dependent on the transmission of information among billions of neurons. However, potential patterns are hardly discoverable due to the high dimensionality in neural signals. Previous studies have identified rotary trajectories in rhythm and nonrhythm movements when projecting the neural electrical signals into a two-dimensional space. However, it is unclear how well this analogy holds at the resting state. Given the low-frequency fluctuations noted during spontaneous neural activities using functional magnetic resonance imaging (fMRI), it is natural to hypothesize that the neural response at resting state also shows a periodic trajectory. In this study, we explored the potential patterns in resting state fMRI data at four frequency bands (slow 2–slow 5) on two cohorts, one of which consisted of young and elderly adults and the other of patients with Alzheimer’s disease and normal controls (NC). The jPCA algorithm was applied to reduce the high-dimensional BOLD signal into a two-dimensional space for visualization of the trajectory. The results indicated that the “resting state” is a basic state showing an inherent dynamic pattern with a low frequency and long period during normal aging, with changes appearing in the rotary period at the slow 4 frequency band (0.027–0.073 Hz) during the pathological process of Alzheimer’s disease (AD). These findings expand the original understanding that neural signals can rotate themselves and that motor executive signals consist of neural signals. Meanwhile, the rotary period at band slow 4 may be a physiological marker for AD, and studies of this frequency band may be useful for understanding the potential pathophysiology of AD and ultimately facilitate characterization and auxiliary diagnosis of AD.

[1]  E. Evarts,et al.  Relation of pyramidal tract activity to force exerted during voluntary movement. , 1968, Journal of neurophysiology.

[2]  Xi Chen,et al.  Brain Network Evolution after Stroke Based on Computational Experiments , 2013, PloS one.

[3]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[4]  N. Logothetis What we can do and what we cannot do with fMRI , 2008, Nature.

[5]  Ying Han,et al.  Frequency-dependent changes in the amplitude of low-frequency fluctuations in amnestic mild cognitive impairment: A resting-state fMRI study , 2011, NeuroImage.

[6]  J. Kalaska From intention to action: motor cortex and the control of reaching movements. , 2009, Advances in experimental medicine and biology.

[7]  John J. Renger,et al.  Preface to the Special Issue “Novel Pharmaconeurogenetic Approaches Arising from Progress in Translational Genetics” , 2011, Journal of neurogenetics.

[8]  Shang-Yueh Tsai,et al.  Resting‐State Functional Magnetic Resonance Imaging: The Impact of Regression Analysis , 2015, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[9]  G. Buzsáki,et al.  Inhibition and Brain Work , 2007, Neuron.

[10]  Mani Mina,et al.  Source of low‐frequency fluctuations in functional MRI signal , 2008, Journal of magnetic resonance imaging : JMRI.

[11]  T. Aflalo,et al.  Relationship between Unconstrained Arm Movements and Single-Neuron Firing in the Macaque Motor Cortex , 2007, The Journal of Neuroscience.

[12]  E. DeYoe,et al.  Reduction of physiological fluctuations in fMRI using digital filters , 1996, Magnetic resonance in medicine.

[13]  E. Todorov Direct cortical control of muscle activation in voluntary arm movements: a model , 2000, Nature Neuroscience.

[14]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[15]  Christian Cipriani,et al.  Distinct neural patterns enable grasp types decoding in monkey dorsal premotor cortex , 2014, Journal of neural engineering.

[16]  V. Haughton,et al.  Mapping functionally related regions of brain with functional connectivity MR imaging. , 2000, AJNR. American journal of neuroradiology.

[17]  B. Blankertz,et al.  Neuromuscular electrical stimulation induced brain patterns to decode motor imagery , 2013, Clinical Neurophysiology.

[18]  Roel H. R. Deckers,et al.  Large-amplitude, spatially correlated fluctuations in BOLD fMRI signals during extended rest and early sleep stages. , 2006, Magnetic resonance imaging.

[19]  Dewen Hu,et al.  Default network connectivity decodes brain states with simulated microgravity , 2015, Cognitive Neurodynamics.

[20]  G. Buzsáki,et al.  Natural logarithmic relationship between brain oscillators , 2003 .

[21]  Andrew W. Fitzgibbon,et al.  Direct Least Square Fitting of Ellipses , 1999, IEEE Trans. Pattern Anal. Mach. Intell..

[22]  Karl J. Friston,et al.  The default-mode, ego-functions and free-energy: a neurobiological account of Freudian ideas , 2010, Brain : a journal of neurology.

[23]  Chaogan Yan,et al.  DPARSF: A MATLAB Toolbox for “Pipeline” Data Analysis of Resting-State fMRI , 2010, Front. Syst. Neurosci..

[24]  A. P. Georgopoulos,et al.  Neuronal population coding of movement direction. , 1986, Science.

[25]  Alzheimer's Disease Neuroimaging Initiative,et al.  Frequency Specific Effects of ApoE ε4 Allele on Resting-State Networks in Nondemented Elders , 2017, BioMed research international.

[26]  M. Lowe,et al.  Functional Connectivity in Single and Multislice Echoplanar Imaging Using Resting-State Fluctuations , 1998, NeuroImage.

[27]  N. Bargalló,et al.  Changes in whole-brain functional networks and memory performance in aging , 2014, Neurobiology of Aging.

[28]  W. Kristan,et al.  Rhythmic swimming activity in neurones of the isolated nerve cord of the leech. , 1976, The Journal of experimental biology.

[29]  Bharat B. Biswal,et al.  The oscillating brain: Complex and reliable , 2010, NeuroImage.

[30]  P. Fransson Spontaneous low‐frequency BOLD signal fluctuations: An fMRI investigation of the resting‐state default mode of brain function hypothesis , 2005, Human brain mapping.

[31]  J. Haxby,et al.  Localization of Cardiac-Induced Signal Change in fMRI , 1999, NeuroImage.

[32]  R. Buckner,et al.  Human Brain Mapping 6:373–377(1998) � Event-Related fMRI and the Hemodynamic Response , 2022 .

[33]  Yong He,et al.  Disrupted Functional Brain Connectome in Individuals at Risk for Alzheimer's Disease , 2013, Biological Psychiatry.

[34]  Xi Chen,et al.  Point process analysis in brain networks of patients with diabetes , 2014, Neurocomputing.