Breakdown of Long-Range Temporal Correlations in Theta Oscillations in Patients with Major Depressive Disorder

Neuroimaging has revealed robust large-scale patterns of high neuronal activity in the human brain in the classical eyes-closed wakeful rest condition, pointing to the presence of a baseline of sustained endogenous processing in the absence of stimulus-driven neuronal activity. This baseline state has been shown to differ in major depressive disorder. More recently, several studies have documented that despite having a complex temporal structure, baseline oscillatory activity is characterized by persistent autocorrelations for tens of seconds that are highly replicable within and across subjects. The functional significance of these long-range temporal correlations has remained unknown. We recorded neuromagnetic activity in patients with a major depressive disorder and in healthy control subjects during eyes-closed wakeful rest and quantified the long-range temporal correlations in the amplitude fluctuations of different frequency bands. We found that temporal correlations in the theta-frequency band (3-7 Hz) were almost absent in the 5-100 s time range in the patients but prominent in the control subjects. The magnitude of temporal correlations over the left temporocentral region predicted the severity of depression in the patients. These data indicate that long-range temporal correlations in theta oscillations are a salient characteristic of the healthy human brain and may have diagnostic potential in psychiatric disorders. We propose a link between the abnormal temporal structure of theta oscillations in the depressive patients and the systems-level impairments of limbic-cortical networks that have been identified in recent anatomical and functional studies of patients with major depressive disorder.

[1]  V. Knott,et al.  EEG power, frequency, asymmetry and coherence in male depression , 2001, Psychiatry Research: Neuroimaging.

[2]  Shlomo Havlin,et al.  Scaling behaviour of heartbeat intervals obtained by wavelet-based time-series analysis , 1996, Nature.

[3]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[4]  R. Parenti,et al.  Expression of connexin36 mRNA in adult rodent brain , 2000, Neuroreport.

[5]  K. Linkenkaer-Hansen,et al.  Long-Range Temporal Correlations and Scaling Behavior in Human Brain Oscillations , 2001, The Journal of Neuroscience.

[6]  M. Raichle,et al.  Subgenual prefrontal cortex abnormalities in mood disorders , 1997, Nature.

[7]  G. Buzsáki Theta Oscillations in the Hippocampus , 2002, Neuron.

[8]  K. Linkenkaer-Hansen,et al.  Stimulus‐induced change in long‐range temporal correlations and scaling behaviour of sensorimotor oscillations , 2004, The European journal of neuroscience.

[9]  C. J Stam,et al.  Brain dynamics in theta and alpha frequency bands and working memory performance in humans , 2000, Neuroscience Letters.

[10]  M. Hamilton A RATING SCALE FOR DEPRESSION , 1960, Journal of neurology, neurosurgery, and psychiatry.

[11]  H. Petsche,et al.  Synchronization between prefrontal and posterior association cortex during human working memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[12]  H. Stanley,et al.  Effect of trends on detrended fluctuation analysis. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[13]  E. Castrén,et al.  Is mood chemistry? , 2005, Nature Reviews Neuroscience.

[14]  B. Litt,et al.  Long-range temporal correlations in epileptogenic and non-epileptogenic human hippocampus , 2004, Neuroscience.

[15]  Ian J. Kirk,et al.  The Role of Theta-Range Oscillations in Synchronising and Integrating Activity in Distributed Mnemonic Networks , 2003, Cortex.

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

[17]  Michel Le Van Quyen,et al.  Disentangling the dynamic core: a research program for a neurodynamics at the large-scale. , 2003, Biological research.

[18]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[19]  R. Hari,et al.  Phase locking between human primary and secondary somatosensory cortices , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Mark Lau,et al.  Modulation of cortical-limbic pathways in major depression: treatment-specific effects of cognitive behavior therapy. , 2004, Archives of general psychiatry.

[21]  M M Mesulam,et al.  Report of IFCN Committee on Basic Mechanisms. Basic mechanisms of cerebral rhythmic activities. , 1990, Electroencephalography and clinical neurophysiology.

[22]  K. Linkenkaer-Hansen,et al.  Interhemispheric phase synchrony and amplitude correlation of spontaneous beta oscillations in human subjects: a magnetoencephalographic study , 2001, Neuroreport.

[23]  Bruce S. McEwen,et al.  Course of Illness, Hippocampal Function, and Hippocampal Volume in Major Depression , 2005 .

[24]  H. Stanley,et al.  Quantification of scaling exponents and crossover phenomena in nonstationary heartbeat time series. , 1995, Chaos.

[25]  T. Brismar,et al.  Long-range temporal correlations in electroencephalographic oscillations: Relation to topography, frequency band, age and gender , 2005, Neuroscience.

[26]  Jan W. Kantelhardt,et al.  Modeling transient correlations in heartbeat dynamics during sleep , 2003 .

[27]  A. Kleinschmidt,et al.  Electroencephalographic signatures of attentional and cognitive default modes in spontaneous brain activity fluctuations at rest , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Michael Marriott,et al.  Lower hippocampal volume in patients suffering from depression: a meta-analysis. , 2004, The American journal of psychiatry.

[29]  W. Drevets Neuroimaging studies of mood disorders , 2000, Biological Psychiatry.

[30]  Wolf Singer,et al.  Neuronal Synchrony: A Versatile Code for the Definition of Relations? , 1999, Neuron.

[31]  R. Eckhorn,et al.  Amplitude envelope correlation detects coupling among incoherent brain signals , 2000, Neuroreport.

[32]  W. Heller,et al.  The puzzle of regional brain activity in depression and anxiety: The importance of subtypes and comorbidity. , 1998 .

[33]  A. Goldberger Non-linear dynamics for clinicians: chaos theory, fractals, and complexity at the bedside , 1996, The Lancet.

[34]  H. Mayberg Modulating dysfunctional limbic-cortical circuits in depression: towards development of brain-based algorithms for diagnosis and optimised treatment. , 2003, British medical bulletin.

[35]  F. L. D. Silva,et al.  Basic mechanisms of cerebral rhythmic activities , 1990 .

[36]  J. Karhu,et al.  Theta oscillations index human hippocampal activation during a working memory task. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[37]  M. Kahana,et al.  Theta returns , 2001, Current Opinion in Neurobiology.

[38]  N. Logothetis,et al.  Very slow activity fluctuations in monkey visual cortex: implications for functional brain imaging. , 2003, Cerebral cortex.

[39]  G. Goodwin,et al.  Cognitive deficits in depression: Possible implications for functional neuropathology , 2001, British Journal of Psychiatry.

[40]  L. Pelosi,et al.  Working memory dysfunction in major depression: an event-related potential study , 2000, Clinical Neurophysiology.

[41]  L. Glass Synchronization and rhythmic processes in physiology , 2001, Nature.

[42]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[43]  Ivanov PCh,et al.  Application of statistical physics to heartbeat diagnosis. , 1999, Physica A.

[44]  C D Tesche,et al.  Signal-space projections of MEG data characterize both distributed and well-localized neuronal sources. , 1995, Electroencephalography and clinical neurophysiology.

[45]  Jeffrey M. Hausdorff,et al.  Fractal dynamics in physiology: Alterations with disease and aging , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[46]  T. Brismar,et al.  Long-range temporal correlations in alpha and beta oscillations: effect of arousal level and test–retest reliability , 2004, Clinical Neurophysiology.

[47]  A. N. Mamelak,et al.  Long-range temporal correlations in the spontaneous spiking of neurons in the hippocampal-amygdala complex of humans , 2005, Neuroscience.

[48]  W. Drevets,et al.  The cellular neurobiology of depression , 2001, Nature Medicine.