Abstract
Abnormal long-range temporal correlation (LRTC) in EEG oscillation has been observed in several brain pathologies and mental disorders. This study examined the relationship between the LRTC of broadband EEG oscillation and depression following cerebral infarction with different hemispheric lesions to provide a novel insight into such depressive disorders. Resting EEGs of 16 channels in 18 depressed (9 left and 9 right lesions) and 21 non-depressed (11 left and 10 right lesions) subjects following cerebral infarction and 19 healthy control subjects were analysed by means of detrended fluctuation analysis, a quantitative measurement of LRTC. The difference among groups and the correlation between the severity of depression and LRTC in EEG oscillation were investigated by statistical analysis. The results showed that LRTC of broadband EEG oscillations in depressive subjects was still preserved but attenuated in right hemispheric lesion subjects especially in left pre-frontal and right inferior frontal and posterior temporal regions. Moreover, an association between the severity of psychiatric symptoms and the attenuation of the LRTC was found in frontal, central and temporal regions for stroke subjects with right lesions. A high discriminating ability of the LRTC in the frontal and central regions to distinguish depressive from non-depressive subjects suggested potential feasibility for LRTC as an assessment indicator for depression following right hemispheric cerebral infarction. Different performance of temporal correlation in depressed subjects following the two hemispheric lesions implied complex association between depression and stroke lesion location.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
American Electroencephalographic Society (1994) Guideline thirteen: guidelines for standard electrode position nomenclature. J Clin Neurophysiol 11:111–113
American Psychiatric Association (1994) Diagnostic and statistical manual of mental disorders, 4 (DSM-IV) edn. American Psychiatric Association, Washington
Beggs JM, Plenz D (2003) Neuronal avalanches in neocortical circuits. J Neurosci 23:11167–11177
Berg A, Palomäki H, Lehtihalmes M et al (2001) Poststroke depression in acute phase after stroke. Cerebrovasc Dis 12:14–20. doi:10.1159/000047675
Berg A, Palomäki H, Lehtihalmes M et al (2003) Poststroke depression: an 18-month follow-up. Stroke 34:138–143. doi:10.1161/01.STR.0000048149.84268.07
Bhogal SK, Teasell R, Foley N, Speechley M (2004) Lesion location and poststroke depression: systematic review of the methodological limitations in the literature. Stroke 35:794–802. doi:10.1161/01.STR.0000117237.98749.26
Bogousslavsky J (2003) William Feinberg lecture 2002: emotions, mood, and behavior after stroke. Stroke 34:1046–1050. doi:10.1161/01.STR.0000061887.33505.B9
Bornas X, Noguera M, Balle M et al (2013) Long-range temporal correlations in resting EEG: its associations with depression-related emotion regulation strategies. J Psychophysiol 27:60–66. doi:10.1027/0269-8803/a000087
Bornas X, Fiol-Veny A, Balle M et al (2015) Long range temporal correlations in EEG oscillations of subclinically depressed individuals: their association with brooding and suppression. Cogn Neurodyn 9:53–62. doi:10.1007/s11571-014-9313-1
Bowers D, Blonder LX, Feinberg T, Heilman KM (1991) Differential impact of right and left hemisphere lesions on facial emotion and object imagery. Brain 114:2593–2609. doi:10.1093/brain/114.6.2593
Carson AJ, MacHale S, Allen K et al (2000) Depression after stroke and lesion location: a systematic review. Lancet 356:122–126. doi:10.1016/S0140-6736(00)02448-X
Chemerinski E, Robinson RG, Kosier JT (2001) Improved recovery in activities of daily living associated with remission of poststroke depression. Stroke 32:113–117. doi:10.1161/01.STR.32.1.113
de Coster L, Leentjens AFG, Lodder J, Verhey FRJ (2005) The sensitivity of somatic symptoms in post-stroke depression: a discriminant analytic approach. Int J Geriatr Psychiatry 20:358–362. doi:10.1002/gps.1290
De Man-Van Ginkel JM, Hafsteinsdóttir TB, Lindeman E et al (2013) In-hospital risk prediction for post-stroke depression: development and validation of the post-stroke depression prediction scale. Stroke 44:2441–2445. doi:10.1161/STROKEAHA.111.000304
Denny-brown D, Meyer JS, Horenstein S (1952) The significance of perceptual rivalry resulting from parietal lesion. Brain 75:432–471. doi:10.1093/brain/75.4.432
Dimitriadis SI, Laskaris NA, Micheloyannis S (2015) Transition dynamics of EEG-based network microstates during mental arithmetic and resting wakefulness reflects task-related modulations and developmental changes. Cogn Neurodyn 9:371–387. doi:10.1007/s11571-015-9330-8
Fields C, Glazebrook JF (2017) Disrupted development and imbalanced function in the global neuronal workspace: a positive-feedback mechanism for the emergence of ASD in early infancy. Cogn Neurodyn 11:1–21. doi:10.1007/s11571-016-9419-8
Fingelkurts AA, Fingelkurts AA (2015) Altered structure of dynamic electroencephalogram oscillatory pattern in major depression. Biol Psychiatry 77:1050–1060. doi:10.1016/j.biopsych.2014.12.011
Fiol-Veny A, Balle M, Bornas X (2015) Long range temporal correlations in EEG and depression. Ann Depress Anxiety 2:1–5
Florin E, Baillet S (2015) The brain’s resting-state activity is shaped by synchronized cross-frequency coupling of neural oscillations. Neuroimage 111:26–35. doi:10.1016/j.neuroimage.2015.01.054
Gaete JM, Bogousslavsky J (2008) Post-stroke depression. Expert Rev Neurother 8:75–92. doi:10.1586/14737175.8.1.75
Gutiérrez D, Ramírez-Moreno MA (2016) Assessing a learning process with functional ANOVA estimators of EEG power spectral densities. Cogn Neurodyn 10:175–183. doi:10.1007/s11571-015-9368-7
Hamilton M (1960) A rating scale for depression. J Neurol Neurosurg Psychiatry 23:56–62. doi:10.1136/jnnp.23.1.56
Hecht D (2010) Depression and the hyperactive right-hemisphere. Neurosci Res 68:77–87. doi:10.1016/j.neures.2010.06.013
Herrmann M, Bartels C, Schumacher M, Wallesch CW (1995) Poststroke depression. Is there a pathoanatomic correlate for depression in the postacute stage of stroke? Stroke 26:850–856
House A, Dennis M, Warlow C et al (1990) Mood disorders after stroke and their relation to lesion location. A CT scan study. Brain 113(Pt 4):1113–1129
Juhász C, Kamondi A, Szirmai I (1997) Spectral EEG analysis following hemispheric stroke. Acta Neurol Scand 96:397–400. doi:10.1111/j.1600-0404.1997.tb00305.x
Karkare S, Saha G, Bhattacharya J (2009) Investigating long-range correlation properties in EEG during complex cognitive tasks. Chaos Solitons Fractals 42:2067–2073. doi:10.1016/j.chaos.2009.03.148
Lee JS, Yang BH, Lee JH et al (2007) Detrended fluctuation analysis of resting EEG in depressed outpatients and healthy controls. Clin Neurophysiol 118:2489–2496. doi:10.1016/j.clinph.2007.08.001
Leistedt S, Dumont M, Coumans N et al (2007a) The modifications of the long-range temporal correlations of the sleep EEG due to major depressive episode disappear with the status of remission. Neuroscience 148:782–793. doi:10.1016/j.neuroscience.2007.06.032
Leistedt S, Dumont M, Lanquart JP et al (2007b) Characterization of the sleep EEG in acutely depressed men using detrended fluctuation analysis. Clin Neurophysiol 118:940–950. doi:10.1016/j.clinph.2007.01.003
Li Y, Qiu J, Yan R et al (2008) Weakened long-range correlation of renal sympathetic nerve activity in Wistar rats after anaesthesia. Neurosci Lett 433:28–32. doi:10.1016/j.neulet.2007.12.038
Linkenkaer-Hansen K, Nikouline VV, Palva JM et al (2001) Long-range temporal correlations and scaling behavior in human brain oscillations. J Neurosci 21:1370–1377
Linkenkaer-Hansen K, Monto S, Rytsälä H et al (2005) Breakdown of long-range temporal correlations in theta oscillations in patients with major depressive disorder. J Neurosci 25:10131–10137. doi:10.1523/JNEUROSCI.3244-05.2005
Linkenkaer-Hansen K, Smit D, Barkil A et al (2007) Genetic contributions to long-range temporal correlations in ongoing oscillations. J Neurosci 27:13882–13889. doi:10.1523/JNEUROSCI.3083-07.2007
Montez T, Poil S-S, Jones BF et al (2009) Altered temporal correlations in parietal alpha and prefrontal theta oscillations in early-stage Alzheimer disease. Proc Natl Acad Sci USA 106:1614–1619. doi:10.1073/pnas.0811699106
Nikulin VV, Brismar T (2004) Long-range temporal correlations in alpha and beta oscillations: effect of arousal level and test-retest reliability. Clin Neurophysiol 115:1896–1908. doi:10.1016/j.clinph.2004.03.019
Nikulin VV, Brismar T (2005) Long-range temporal correlations in electroencephalographic oscillations: relation to topography, frequency band, age and gender. Neuroscience 130:549–558. doi:10.1016/j.neuroscience.2004.10.007
Nikulin VV, Jönsson EG, Brismar T (2012) Attenuation of long-range temporal correlations in the amplitude dynamics of alpha and beta neuronal oscillations in patients with schizophrenia. Neuroimage 61:162–169. doi:10.1016/j.neuroimage.2012.03.008
Paradiso S, Vaidya J, Tranel D (2008) Nondysphoric depression following stroke. The Journal of neuropsychiatry and clinical neurosciences 20(1):52–61. doi:10.1176/jnp.2008.20.1.52
Pedroso VSP, de Souza LC, Brunoni AR, Teixeira AL (2015) Post stroke depression: clinics, etiopathogenesis and therapeutics. Rev Psiquiatr Clin 42:18–24. doi:10.1590/0101-60830000000041
Peng CK, Havlin S, Stanley HE, Goldberger AL (1995) Quantification of scaling exponents and crossover phenomena in nonstationary heartbeat time series. Chaos 5:82–87. doi:10.1017/CBO9781107415324.004
Pu J, Xu H, Wang Y et al (2016) Combined nonlinear metrics to evaluate spontaneous EEG recordings from chronic spinal cord injury in a rat model: a pilot study. Cogn Neurodyn 10:1–7. doi:10.1007/s11571-016-9394-0
Qu J, Wang R, Yan C et al (2014) Oscillations and synchrony in a cortical neural network. Cogn Neurodyn 8(2):157–166. doi:10.1007/s11571-013-9268-7
Robinson R (2003) Poststroke depression: prevalence, diagnosis, treatment, and disease progression. Biol Psychiatry 54:376–387. doi:10.1016/S0006-3223(03)00423-2
Robinson RG (2006) The clinical neuropsychiatry of stroke. Cambridge University Press, New York
Robinson RG, Coyle JT (1980) The differential effect of right versus left hemispheric cerebral infarction on catecholamines and behavior in the rat. Brain Res 188:63–78. doi:10.1016/0006-8993(80)90557-0
Robinson RG, Starkstein SE (1989) Mood disorders following stroke: new findings and future directions. J Geriatr Psychiatry 22:1–15
Singh A, Black SE, Herrmann N et al (2000) Functional and neuroanatomic correlations in poststroke depression: the Sunnybrook stroke study. Stroke 31:637–644. doi:10.1161/01.STR.31.3.637
Sinyor D, Jacques P, Kaloupek DG et al (1986) Poststroke depression and lesion location: an attempted replication. Brain 109:537–546. doi:10.1093/brain/109.3.537
Smit DJ, de Geus EJ, van de Nieuwenhuijzen ME et al (2011) Scale-free modulation of resting-state neuronal oscillations reflects prolonged brain maturation in humans. J Neurosci 31:13128–13136. doi:10.1523/JNEUROSCI.1678-11.2011
Spalletta G, Serra L, Fadda L et al (2007) Unawareness of motor impairment and emotions in right hemispheric stroke: a preliminary investigation. Int J Geriatr Psychiatry 22:1241–1246. doi:10.1002/gps.1822
Stam CJ, de Bruin EA (2004) Scale-free dynamics of global functional connectivity in the human brain. Hum Brain Mapp 22:97–109
Takahashi T, Cho RY, Murata T et al (2009) Age-related variation in EEG complexity to photic stimulation: a multiscale entropy analysis. Clin Neurophysiol 120:476–483. doi:10.1016/j.clinph.2008.12.043
Wang CF, Chen YY, Zhang Y et al (2017) Quantitative EEG abnormalities in major depressive disorder with basal ganglia stroke with lesions in different hemispheres. J Affect Disord 215:172–178. doi:10.1016/j.jad.2017.02.030
Yuvaraj R, Murugappan M (2016) Hemispheric asymmetry non-linear analysis of EEG during emotional responses from idiopathic Parkinson’s disease patients. Cogn Neurodyn 10:225–234. doi:10.1007/s11571-016-9375-3
Zhang T, Jing X, Zhao X et al (2012) Depression after stroke and lesion location: a systematic review. J Affect Disord 136:e83–e87. doi:10.1016/j.jad.2011.06.014
Zhang Y, Wang C, Sun C, et al (2015) Neural complexity in patients with poststroke depression: a resting EEG study. J Affect Disord 188:310–318. doi:10.1016/j.jad.2015.09.017
Acknowledgement
This work was supported by Tianjin Municipal Commission of Health and Family Planning, Tianjin, China (14KG107, 2012KZ044).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
None of the authors have potential conflicts of interest to be disclosed.
Rights and permissions
About this article
Cite this article
Hou, D., Wang, C., Chen, Y. et al. Long-range temporal correlations of broadband EEG oscillations for depressed subjects following different hemispheric cerebral infarction. Cogn Neurodyn 11, 529–538 (2017). https://doi.org/10.1007/s11571-017-9451-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11571-017-9451-3