Association of specific frequency bands of functional MRI signal oscillations with motor symptoms and depression in Parkinson’s disease

A novel empirical mode decomposition method was adopted to investigate the dissociative or interactive neural impact of depression and motor impairments in Parkinson’s disease (PD). Resting-state fMRI data of 59 PD subjects were first decomposed into characteristic frequency bands, and the main effects of motor severity and depression and their interaction on the energy of blood-oxygen-level-dependent signal oscillation in specific frequency bands were then evaluated. The results show that the severity of motor symptoms is negatively correlated with the energy in the frequency band of 0.10–0.25 Hz in the bilateral thalamus, but positively correlated with 0.01–0.027 Hz band energy in the bilateral postcentral gyrus. The severity of depression, on the other hand, is positively correlated with the energy of 0.10–0.25 Hz but negatively with 0.01–0.027 Hz in the bilateral subgenual gyrus. Notably, the interaction between motor and depressive symptoms is negatively correlated with the energy of 0.10–0.25 Hz in the substantia nigra, hippocampus, inferior orbitofrontal cortex, and temporoparietal junction, but positively correlated with 0.02–0.05 Hz in the same regions. These findings indicate unique associations of fMRI band signals with motor and depressive symptoms in PD in specific brain regions, which may underscore the neural impact of the comorbidity and the differentiation between the two PD-related disorders.

[1]  P. Pahapill,et al.  Deep brain stimulation for Parkinson's disease dissociates mood and motor circuits: A functional MRI case study , 2003, Movement disorders : official journal of the Movement Disorder Society.

[2]  A. Cools,et al.  Evidence for lateral premotor and parietal overactivity in Parkinson's disease during sequential and bimanual movements. A PET study. , 1998, Brain : a journal of neurology.

[3]  Roland N. Boubela,et al.  Beyond Noise: Using Temporal ICA to Extract Meaningful Information from High-Frequency fMRI Signal Fluctuations during Rest , 2013, Front. Hum. Neurosci..

[4]  Dennis J. L. G. Schutter,et al.  The cerebellum on the rise in human emotion , 2008, The Cerebellum.

[5]  Yihong Yang,et al.  Frequency specificity of functional connectivity in brain networks , 2008, NeuroImage.

[6]  Yi Zhang,et al.  Frequency Specificity of Regional Homogeneity in the Resting-State Human Brain , 2014, PloS one.

[7]  Y. Liu,et al.  Apathy, depression, and motor symptoms have distinct and separable resting activity patterns in idiopathic Parkinson disease , 2013, NeuroImage.

[8]  Y. Parmet,et al.  EEG frequency analysis in demented and nondemented parkinsonian patients. , 1994, Dementia.

[9]  Alexis T Baria,et al.  Anatomical and Functional Assemblies of Brain BOLD Oscillations , 2011, The Journal of Neuroscience.

[10]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[11]  C. Beckmann,et al.  Spectral characteristics of resting state networks. , 2011, Progress in brain research.

[12]  Eric J. Nestler,et al.  The molecular neurobiology of depression , 2008, Nature.

[13]  Zhizhong Wang,et al.  Mean frequency derived via Hilbert-Huang transform with application to fatigue EMG signal analysis , 2006, Comput. Methods Programs Biomed..

[14]  Huafu Chen,et al.  Is there a cerebellar compensatory effort in first-episode, treatment-naive major depressive disorder at rest? , 2013, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[15]  Yonggui Yuan,et al.  Abnormal functional connectivity of the amygdala is associated with depression in Parkinson's disease , 2015, Movement disorders : official journal of the Movement Disorder Society.

[16]  O. Sinanović,et al.  EEG frequency and cognitive dysfunction in patients with Parkinson's disease. , 2005, Medicinski arhiv.

[17]  H. Mayberg,et al.  Depression in Parkinson's disease: a biochemical and organic viewpoint. , 1995, Advances in neurology.

[18]  H. Mayberg,et al.  Selective hypometabolism in the inferior frontal lobe in depressed patients with Parkinson's disease , 1990, Annals of neurology.

[19]  Kielan Yarrow,et al.  Modulation of subthalamic alpha activity to emotional stimuli correlates with depressive symptoms in Parkinson's disease 1 , 2011, Movement disorders : official journal of the Movement Disorder Society.

[20]  Uwe Walter,et al.  Parkinson's disease-like midbrain sonography abnormalities are frequent in depressive disorders. , 2007, Brain : a journal of neurology.

[21]  D J Brooks,et al.  Advances in imaging Parkinson's disease. , 1997, Current opinion in neurology.

[22]  David Eidelberg,et al.  Relationships among the metabolic patterns that correlate with mnemonic, visuospatial, and mood symptoms in Parkinson's disease. , 2002, The American journal of psychiatry.

[23]  Vladimir Litvak,et al.  Synchronized neural oscillations and the pathophysiology of Parkinson's disease. , 2013, Current opinion in neurology.

[24]  H. Soininen,et al.  Slowing of EEG in Parkinson's disease. , 1991, Electroencephalography and clinical neurophysiology.

[25]  U. Bonuccelli,et al.  Psychiatric comorbidity in a population of Parkinson's disease patients , 2004, European journal of neurology.

[26]  Piero Antuono,et al.  Neural basis of the association between depressive symptoms and memory deficits in nondemented subjects: resting‐state fMRI study , 2012, Human brain mapping.

[27]  M. Garolera,et al.  Depression in Parkinson's disease: clinical correlates and outcome. , 2003, Parkinsonism & related disorders.

[28]  Hong Yu,et al.  Role of hyperactive cerebellum and motor cortex in Parkinson's disease , 2007, NeuroImage.

[29]  Dag Aarsland,et al.  Depression in Parkinson disease—epidemiology, mechanisms and management , 2011, Nature Reviews Neurology.

[30]  Danny C. W. Chan,et al.  Therapeutic Deep Brain Stimulation in Parkinsonian Rats Directly Influences Motor Cortex , 2012, Neuron.

[31]  A. Schrag,et al.  Psychosis, apathy, depression and anxiety in Parkinson's disease , 2012, Neurobiology of Disease.

[32]  Clement Hamani,et al.  The Subcallosal Cingulate Gyrus in the Context of Major Depression , 2011, Biological Psychiatry.

[33]  Fabrizio Esposito,et al.  Rhythm-specific modulation of the sensorimotor network in drug-naive patients with Parkinson's disease by levodopa. , 2013, Brain : a journal of neurology.

[34]  N. Huang,et al.  The empirical mode decomposition and the Hilbert spectrum for nonlinear and non-stationary time series analysis , 1998, Proceedings of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[35]  Hsin-Yi Lai,et al.  Functional MRI reveals frequency-dependent responses during deep brain stimulation at the subthalamic nucleus or internal globus pallidus , 2014, NeuroImage.

[36]  Anthony R. McIntosh,et al.  Limbic–frontal circuitry in major depression: a path modeling metanalysis , 2004, NeuroImage.

[37]  V. Giampietro,et al.  Fronto-Striato-Cerebellar Dysregulation in Adolescents with Depression During Motivated Attention , 2012, Biological Psychiatry.

[38]  M. Hallett,et al.  Lateralization of brain activity pattern during unilateral movement in Parkinson's disease , 2015, Human brain mapping.

[39]  F. Verhey,et al.  The validity of the Hamilton and Montgomery‐Åsberg depression rating scales as screening and diagnostic tools for depression in Parkinson's disease , 2000, International journal of geriatric psychiatry.

[40]  David J. Brooks,et al.  Imaging biomarkers in Parkinson's disease , 2011, Progress in Neurobiology.