Skip to main content
SpringerLink
Log in

Decrease of theta response in euthymic bipolar patients during an oddball paradigm

  • Research Article
  • Published:
Cognitive Neurodynamics Aims and scope Submit manuscript

Abstract

Theta oscillations are related to cognitive functions and reflect functional integration of frontal and medial temporal structures into coherent neurocognitive networks. This study assessed event-related theta oscillations in medication-free, euthymic patients with bipolar disorder upon auditory oddball paradigm. Twenty-two DSM-IV euthymic bipolar I (n = 19) and II (n = 3) patients and twenty-two healthy subjects were included. Patients were euthymic for at least 6 months, and psychotropic-free for at least 2 weeks. EEG was recorded at 30 electrode sites. Auditory oddball paradigm and sensory stimuli were used. Event-related Oscillations were analyzed using adaptive filtering in two different theta frequency bands (4–6 Hz, 6–8 Hz). In healthy subjects, slow theta (4–6 Hz) responses were significantly higher than those of euthymic patients upon target, non-target and sensory stimuli (p < 0.05). Fast theta (6–8 Hz) responses of healthy subjects were significantly higher than those of euthymic patients upon target-only stimuli (p < 0.05). Reduced theta oscillations during auditory processing provide strong quantitative evidence of activation deficits in related networks in bipolar disorder. Fast theta responses are related to cognitive functions, whereas slow theta responses are related to sensory processes more than cognitive processes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aftanas LI, Golocheikine SA (2001) Human anterior and frontal midline theta and lower alpha reflect emotionally positive state and internalized attention: high-resolution EEG investigation of meditation. Neurosci Lett 310:57–60

    Article  PubMed  CAS  Google Scholar 

  • Aftanas L, Varlamov A, Pavlov S, Makhnev V, Reva N (2001) Event-related synchronization and desynchronization during affective processing: emergence of valence-related time-dependent hemispheric asymmetries in theta and upper alpha band. Int J Neurosci 110:197–219

    Article  PubMed  CAS  Google Scholar 

  • Aftanas LI, Pavlov SV, Reva NV, Varlamov AA (2003a) Trait anxiety impact on the EEG theta band power changes during appraisal of threatening and pleasant visual stimuli. Int J Psychophysiol 50:205–212

    Article  PubMed  Google Scholar 

  • Aftanas LI, Varlamov AA, Reva NV, Pavlov SV (2003b) Disruption of early event-related theta synchronization of human EEG in alexithymics viewing affective pictures. Neurosci Lett 340:57–60

    Article  PubMed  CAS  Google Scholar 

  • Aydemir Ö, Deveci A (2003) Validity and reliability of structured interview for Hamilton depression rating scale seasonal affective disorders version. VIIth annual spring symposium of psychiatric association of Türkiye abstract book, p 187

  • Başar E (1998) Brain oscillations I: principles and approaches. Springer, Heidelberg

    Google Scholar 

  • Başar E (1999) Brain function and oscillations: II. Integrative brain function. Neurophysiology and cognitive processes. Springer, Heidelberg

    Google Scholar 

  • Başar E (2004) Memory and brain dynamics: oscillations integrating attention, perception, learning and memory. CRC Press, Florida

    Google Scholar 

  • Başar E (2006) The theory of whole-brain-work. Int J Psychophysiol 60:133–138

    Article  PubMed  Google Scholar 

  • Başar E (2010) Why the concept of “Quantum Brain” was not discovered in 1940 s. NeuroQuantology 8:322–336

    Google Scholar 

  • Başar E, Güntekin B (2008) A review of brain oscillations in cognitive disorders and the role of neurotransmitters. Brain Res 1235:172–193

    Article  PubMed  Google Scholar 

  • Başar E, Schürmann M, Sakowitz O (2001) The selectively distributed theta system: functions. Int J Psychophysiol 39:197–212

    Article  PubMed  Google Scholar 

  • Başar E, Güntekin B, Tülay E, Yener GG (2010) Evoked and event-related coherence of alzheimer patients manifest differentiation of sensory-cognitive networks. Brain Res 1357:79–90

    Article  PubMed  Google Scholar 

  • Başar E, Güntekin B, Atagün İ, Turp Gölbaşı B, Tülay E, Özerdem A (2012) Brain’s alpha activity is highly reduced in euthymic bipolar disorder patients. Cogn Neurodyn 6:11–20

    Article  PubMed  Google Scholar 

  • Başar-Eroğlu C, Başar E (1991) A compound P300–40 Hz response of the cat hippocampus. Int J Neurosci 60:227–237

    PubMed  Google Scholar 

  • Başar-Eroğlu C, Demiralp T (2001) Event-related theta oscillations: an integrative and comparative approach in the human and animal Brain. Int J Psychophysiol 39:167–195

    Article  PubMed  Google Scholar 

  • Başar-Eroğlu C, Başar E, Demiralp T, Schürmann M (1992) P300-response: possible psychophysiological correlates in delta and theta frequency channels. A review. Int J Psychophysiol 13:161–179

    Article  PubMed  Google Scholar 

  • Başar-Eroğlu C, Schmiedt-Fehr C, Marbach S, Brand A, Mathes B (2008) Altered oscillatory alpha and theta networks in schizophrenia. Brain Res 1235:143–152

    Article  PubMed  Google Scholar 

  • Bhattacharya J (2001) Reduced degree of long-range phase synchrony in pathological human brain. Acta Neurobiol Exp (Wars) 61:309–318

    CAS  Google Scholar 

  • Blumberg HP, Charney DS, Krystal JH (2002) Frontotemporal neural systems in bipolar disorder. Semin Clin Neuropsychiatry 7:243–254

    Article  PubMed  Google Scholar 

  • Bora E, Yucel M, Pantelis C (2009) Cognitive endophenotypes of bipolar disorder: a meta-analysis of neuropsychological deficits in euthymic patients and their first-degree relatives. J Affect Disord 113:1–20

    Article  PubMed  Google Scholar 

  • Boucher R, Bryden MP (1997) Laterality effects in the processing of melody and timbre. Neuropsychologia 35:1467–1473

    Article  PubMed  CAS  Google Scholar 

  • Caligiuri MP, Brown GG, Meloy MJ, Eyler LT, Kindermann SS, Eberson S, Frank LR, Lohr JB (2004) A functional magnetic resonance imaging study of cortical asymmetry in bipolar disorder. Bipolar Disord 6:183–196

    Article  PubMed  Google Scholar 

  • Caravaglios G, Castro G, Costanzo E, Di Maria G, Mancuso D, Muscoso EG (2010) θ power responses in mild Alzheimer’s disease during an auditory oddball paradigm: lack of theta enhancement during stimulus processing. J Neural Transm 117:1195–1208

    Article  PubMed  Google Scholar 

  • Chen AC, Tang Y, Rangaswamy M, Wang JC, Almasy L, Foroud T, Edenberg HJ, Hesselbrock V, Nurnberger J Jr, Kuperman S, O’Connor SJ, Schuckit MA, Bauer LO, Tischfield J, Rice JP, Bierut L, Goate A, Porjesz B (2009) Association of single nucleotide polymorphisms in a glutamate receptor gene (GRM8) with theta power of event-related oscillations and alcohol dependence. Am J Med Genet B Neuropsychiatr Genet 150:359–368

    Google Scholar 

  • Demiralp T, Başar E (1992) Theta rhythmicities following expected visual and auditory targets. Int J Psychophysiol 13:147–160

    Article  PubMed  CAS  Google Scholar 

  • Dupont RM, Jernigan TL, Heindel W, Butters N, Shafer K, Wilson T, Hesselink J, Gillin JC (1995) Magnetic resonance imaging and mood disorders. Localization of white matter and other subcortical abnormalities. Arch Gen Psychiatry 52:747–755

    Article  PubMed  CAS  Google Scholar 

  • El-Badri SM, Ashton CH, Moore PB, Mursh VR, Ferrier IN (2001) Electrophysiological and cognitive function in young euthymic patients with bipolar affective disorder. Bipolar Disord 3:79–87

    Article  PubMed  CAS  Google Scholar 

  • First MB, Gibbon M, Spitzer RL, Gibbon M, Williams JBW (1996) User’s guide for the structured interview for DSM-IV axis I disorders—research version (SCID-I, version 2.0, February 1996 final version). Biometrics Research, New York

    Google Scholar 

  • Fridberg DJ, Hetrick WP, Brenner CA, Shekhar A, Steffen AN, Malloy FW, O’Donnell BF (2009) Relationships between auditory event-related potentials and mood state, medication, and comorbid psychiatric illness in patients with bipolar disorder. Bipolar Disord 11:857–866

    Article  PubMed  Google Scholar 

  • Gevins A, Smith ME, McEvoy L, Yu D (1997) High-resolution EEG mapping of cortical activation related to working memory: effects of task difficulty, type of processing, and practice. Cereb Cortex 7:374–385

    Article  PubMed  CAS  Google Scholar 

  • Hall MH, Rijsdijk F, Picchioni M, Schulze K, Ettinger U, Toulopoulou T, Bramon E, Murray RM, Sham P (2007) Substantial shared genetic influences on schizophrenia and event-related potentials. Am J Psychiatry 164:804–812

    Article  PubMed  Google Scholar 

  • Hamilton M (1960) A rating scale for depression. J Neurol Neurosurg Psychiatry 23:56–62

    Article  PubMed  CAS  Google Scholar 

  • Kahana MJ, Sekuler R, Caplan JB, Kirschen M, Madsen JR (1999) Human theta oscillations exhibit task dependence during virtual maze navigation. Nature 399:781–784

    Article  PubMed  CAS  Google Scholar 

  • Kamarajan C, Rangaswamy M, Chorlian DB, Manz N, Tang Y, Pandey AK, Roopesh BN, Stimus AT, Porjesz B (2008) Theta oscillations during the processing of monetary loss and gain: a perspective on gender and impulsivity. Brain Res 1235:45–62

    Article  PubMed  CAS  Google Scholar 

  • Karadağ F, Oral ET, Yalçın FA, Erten E (2002) Validity, Reliability of young mania rating scale in Turkey. Turk Psikiyatri Derg 13:107–114

    PubMed  Google Scholar 

  • Kaya E, Aydemir O, Selcuki D (2007) Residual symptoms in bipolar disorder: the effect of the last episode after remission. Biol Psychiatry 31:1387–1392

    Google Scholar 

  • Kirk IJ, Mackay JC (2003) The role of theta-range oscillations in synchronising and integrating activity in distributed mnemonic networks. Cortex 39:993–1008

    Article  PubMed  Google Scholar 

  • Klimesch W (1999) EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res Brain Res Rev 29:169–195

    Article  PubMed  CAS  Google Scholar 

  • Klimesch W, Doppelmayr M, Russegger H, Pachinger T (1996) Theta band power in the human scalp EEG and the encoding of new information. NeuroReport 7:1235–1240

    Article  PubMed  CAS  Google Scholar 

  • Klimesch W, Doppelmayr M, Pachinger T, Ripper B (1997) Brain oscillations and human memory: EEG correlates in the upper alpha and theta band. Neurosci Lett 238:9–12

    Article  PubMed  CAS  Google Scholar 

  • Klimesch W, Doppelmayr M, Stadler W, Pöllhuber D, Sauseng P, Röhm D (2001a) Episodic retrieval is reflected by a process specific increase in human electroencephalographic theta activity. Neurosci Lett 302:49–52

    Article  PubMed  CAS  Google Scholar 

  • Klimesch W, Doppelmayr M, Yonelinas A, Kroll NE, Lazzara M, Röhm D, Gruber W (2001b) Theta synchronization during episodic retrieval: neural correlates of conscious awareness. Brain Res Cogn Brain Res 12:33–38

    Article  PubMed  CAS  Google Scholar 

  • Krause CM, Sillanmäki L, Koivisto M, Saarela C, Häggqvist A, Laine M, Hämäläinen H (2000) The effects of memory load on event-related EEG desynchronization and synchronization. Clin Neurophysiol 111:2071–2078

    Article  PubMed  CAS  Google Scholar 

  • Lee PS, Chen YS, Hsieh JC, Su TP, Chen LF (2010) Distinct neuronal oscillatory responses between patients with bipolar and unipolar disorders: a magnetoencephalographic study. J Affect Disord 123:270–275

    Article  PubMed  Google Scholar 

  • Lopes da Silva FH (1990) A critical review of clinical applications of topographic mapping of brain potentials. J Clin Neurophysiol 7:535–551

    Article  PubMed  CAS  Google Scholar 

  • Mitchell DJ, McNaughton N, Flanagan D, Kirk IJ (2008) Frontal-midline theta from the perspective of hippocampal “theta”. Prog Neurobiol 86:156–185

    Article  PubMed  Google Scholar 

  • Muir WJ, St Clair DM, Blackwood DH (1991) Long-latency auditory event-related potentials in schizophrenia and in bipolar and unipolar affective disorder. Psychol Med 21:867–879

    Article  PubMed  CAS  Google Scholar 

  • O’Donnell TO, Rotzinger S, Ulrich M, Hanstock CC, Nakashima TT, Silverstone PH (2003) Effects of chronic lithium and sodium valproate on concentrations of brain amino acids. Eur Neuropsychopharmacol 13:220–227

    Article  PubMed  Google Scholar 

  • O’Donnell BF, Hetrick WP, Vohs JL, Krishnan GP, Carroll CA, Shekhar A (2004a) Neural synchronization deficits to auditory stimulation in bipolar disorder. NeuroReport 15:1369–1372

    Article  PubMed  Google Scholar 

  • O’Donnell BF, Vohs JL, Hetrick WP, Carroll CA, Shekhar A (2004b) Auditory event-related potential abnormalities in bipolar disorder and schizophrenia. Int J Psychophysiol 53:45–55

    Article  PubMed  Google Scholar 

  • Onton J, Delorme A, Makeig S (2005) Frontal midline EEG dynamics during working memory. Neuroimage 27:341–356

    Article  PubMed  Google Scholar 

  • Oribe N, Onitsuka T, Hirano S, Hirano Y, Maekawa T, Obayashi C, Ueno T, Kasai K, Kanba S (2010) Differentiation between bipolar disorder and schizophrenia revealed by neural oscillation to speech sounds: an MEG study. Bipolar Disord 12:804–812

    Article  PubMed  Google Scholar 

  • Özerdem A, Güntekin B, Tunca Z, Başar E (2008) Brain oscillatory responses in patients with bipolar disorder manic episode before and after valproate treatment. Brain Res 1235:98–108

    Article  PubMed  Google Scholar 

  • Özerdem A, Güntekin B, Saatçi E, Tunca Z, Başar E (2010) Disturbance in long distance gamma coherence in bipolar disorder. Prog Neuropsychopharmacol Biol Psychiatry 34:861–865

    Article  PubMed  Google Scholar 

  • Özerdem A, Güntekin B, Atagün I, Turp B, Başar E (2011) Reduced long distance gamma (28–48 Hz) coherence in euthymic patients with bipolar disorder. J Affect Disord 132:325–332

    Article  PubMed  Google Scholar 

  • Pantev C, Roberts LE, Elbert T, Ross B, Wienbruch C (1996) Tonotopic organization of the sources of human auditory steady-state responses. Hear Res 101:62–74

    Article  PubMed  CAS  Google Scholar 

  • Paquette C, Bourassa M, Peretz I (1996) Left-ear advantage in pitch perception of complex tones without energy at the fundamental frequency. Neuropsychologia 34:153–157

    Article  PubMed  CAS  Google Scholar 

  • Phillips ML, Drevets WC, Rauch SL, Lane RD (2003) The neurobiology of emotion perception I: towards an understanding of the neural basis of normal emotion perception. Biol Psychiatry 54:504–514

    Article  PubMed  Google Scholar 

  • Raghavachari S, Kahana MJ, Rizzuto DS, Caplan JB, Kirschen MP, Bourgeois B, Madsen JR, Lisman JE (2001) Gating of human theta oscillations by a working memory task. J Neurosci 21:3175–3183

    PubMed  CAS  Google Scholar 

  • Rass O, Krishnan G, Brenner CA, Hetrick WP, Merrill CC, Shekhar A, O’Donnell BF (2010) Auditory steady state response in bipolar disorder: relation to clinical state, cognitive performance, medication status, and substance disorders. Bipolar Disord 12:793–803

    Article  PubMed  Google Scholar 

  • Robinson LJ, Thompson JM, Gallagher P, Goswami U, Young AH, Ferrier IN, Moore PB (2006) A meta-analysis of cognitive deficits in euthymic patients with bipolar disorder. J Affect Disord 93:105–115

    Article  PubMed  Google Scholar 

  • Sakowitz OW, Schürmann M, Başar E (2000) Oscillatory frontal theta responses are increased upon bisensory stimulation. Clin Neurophysiol 111:884–893

    Article  PubMed  CAS  Google Scholar 

  • Salisbury DF, Shenton ME, Sherwood AR, Fischer IA, Yurgelun-Todd DA, Tohen M, McCarley RW (1998) First-episode schizophrenic psychosis differs from first-episode affective psychosis and controls in P300 amplitude over left temporal lobe. Arch Gen Psychiatry 55:173–180

    Article  PubMed  CAS  Google Scholar 

  • Salisbury DF, Shenton ME, McCarley RW (1999) P300 topography differs in schizophrenia and manic psychosis. Biol Psychiatry 45:98–106

    Article  PubMed  CAS  Google Scholar 

  • Sarnthein J, Petsche H, Rappelsberger P, Shaw GL, von Stein A (1998) Synchronization between prefrontal and posterior association cortex during human working memory. Proc Natl Acad Sci USA 95:7092–7096

    Article  PubMed  CAS  Google Scholar 

  • Schulze KK, Hall MH, McDonald C, Marshall N, Walshe M, Murray RM, Bramon E (2007) P50 Auditory Evoked Potential Suppression in Bipolar Unaffected Relatives. Biol Psychiatry 62:121–128

    Article  PubMed  Google Scholar 

  • Schulze KK, Hall MH, McDonald C, Marshall N, Walshe M, Murray RM, Bramon E (2008) Auditory P300 in patients with bipolar disorder and their unaffected relatives. Bipolar Disord 10:377–386

    Article  PubMed  Google Scholar 

  • Souza VB, Muir WJ, Walker MT, Glabus MF, Roxborough HM, Sharp CW, Dunan JR, Blackwood DH (1995) Auditory P300 event-related potentials and neuropsychological performance in schizophrenia and bipolar affective disorder. Biol Psychiatry 37:300–310

    Article  PubMed  CAS  Google Scholar 

  • Strakowski SM, DelBello MP, Adler CM (2005) The functional neuroanatomy of bipolar disorder: a review of neuroimaging findings. Mol Psychiatry 10:105–116

    Article  PubMed  CAS  Google Scholar 

  • Strik WK, Fallgatter AJ, Brandeis D, Pascual-Marqui RD (1998) Three-dimensional tomography of event-related potentials during response inhibition: evidence for phasic frontal lobe activation. Electroencephalogr Clin Neurophysiol 108:406–413

    Article  PubMed  CAS  Google Scholar 

  • von Stein A, Sarnthein J (2000) Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. Int J Psychophysiol 38:301–313

    Article  Google Scholar 

  • Yener G, Başar E (2010) Sensory evoked and event related oscillations in Alzheimer’s disease: a short review. Cogn Neurodyn 4:263–274

    Article  PubMed  Google Scholar 

  • Yener GG, Güntekin B, Oniz A, Başar E (2007) Increased frontal phase-locking of event-related theta oscillations in Alzheimer patients treated with cholinesterase inhibitors. Int J Psychophysiol 64:46–52

    Article  PubMed  CAS  Google Scholar 

  • Young RC, Biggs JT, Ziegler VE, Meyer DA (1978) A rating scale for mania: reliability, validity and sensitivity. Br J Psychiatry 133:429–435

    Article  PubMed  CAS  Google Scholar 

  • Zatorre RJ (2001) Neural specializations for tonal processing. Ann N Y Acad Sci 930:193–210

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Psychiatry, Namik Kemal University Medical School, Tekirdag, Turkey

    M. İ. Atagün

  2. Bakirkoy Research and Training Hospital for Psychiatry Neurology, Neurosurgery, Istanbul, Turkey

    M. İ. Atagün

  3. Brain Dynamics, Cognition and Complex Systems Research Center, Istanbul Kultur University, Istanbul, Turkey

    B. Güntekin, E. Tülay & E. Başar

  4. Department of Psychiatry, Dokuz Eylul University Medical School, Izmir, Turkey

    A. Özerdem

  5. Department of Neuroscience, Dokuz Eylul University Health Sciences Institute, Izmir, Turkey

    A. Özerdem

  6. Multidisciplinary Brain Dynamics Research Center, Dokuz Eylul University, Izmir, Turkey

    A. Özerdem

Authors
  1. M. İ. Atagün
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B. Güntekin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Özerdem
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. Tülay
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. E. Başar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. Başar.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Atagün, M.İ., Güntekin, B., Özerdem, A. et al. Decrease of theta response in euthymic bipolar patients during an oddball paradigm. Cogn Neurodyn 7, 213–223 (2013). https://doi.org/10.1007/s11571-012-9228-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11571-012-9228-7

Keywords

Search

Navigation