Skip to main content

Advertisement

SpringerLink
Log in

Theta responses are abnormal in mild cognitive impairment: evidence from analysis of theta event-related synchronization during a temporal expectancy task

  • Neurology and Preclinical Neurological Studies - Original Article
  • Published:
Journal of Neural Transmission Aims and scope Submit manuscript

Abstract

We examined the hypothesis that the attention/executive deficits in mild cognitive impairment (MCI) due to Alzheimer’s disease is associated to an abnormal cortical activation, revealed by the method of event-related synchronization/desynchronization (ERS/ERD) in the theta band during a paradigm of temporal orienting of attention. MCI patients (n = 25) and healthy elderly (HE) matched controls (n = 15) performed a task in which periodically omitted tones had to be predicted and their virtual onset time had to be marked by pressing a button. Single-trial theta responses were measured, respectively, before and after the motor response. Then, theta responses were compared to theta power during eyes closed resting state (ERD/ERS method).The temporal course of the task was characterized by two different behavioural conditions: (1) a pre-event epoch, in which the subject awaited the virtual onset of the omitted tone, (2) a post-event (after button pressing) epoch, in which the subject was in a post-motor response condition. The most important findings are summarized as follows: (1) in both groups, the pre-event epoch was characterized by theta ERS on temporal electrodes, but HE had a greater theta ERS compared to that of MCI group; (2) in both groups, during the post-motor condition, there was a theta ERS on prefrontal regions, and, also in this case, HE showed a greater theta enhancement compared to that of MCI patients; (3) HE showed evidence of lateralization: during the waiting epoch, theta ERS was dominant on the right posterior temporal lead (T6), whilst, during the post-motor epoch, theta ERS was greater on the left, as well as the midline prefrontal leads. Compared to the traditional neuropsychological measures for the episodic memory, these theta ERS indicators were less accurate in differentiating MCI patients from healthy elderly. The clinical relevance of these findings is that the weaker theta reactivity in MCI would indicate an early impairment in the temporal orienting of attention in the early stage of the clinical course of this neurodegenerative disease.

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
Fig. 5

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

    PubMed  CAS  Google Scholar 

  • Albert MS, DeKosky ST, Dickson D, Dubois B, Feldman HH, Fox NC, Gamst A, Holtzman DM, Jagust WJ, Petersen RC, Snyder PJ, Carrillo MC, Thies B, Phelps CH (2011) The diagnosis of mild cognitive impairment due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimer’s Dement 7:270–279

    Google Scholar 

  • Asada H, Fukuda Y, Tsunoda S, Yamaguchi M, Tonoike M (1999) Frontal midline theta rhythms reflect alternative activation of prefrontal cortex and anterior cingulate cortex in humans. Neurosci Lett 274:29–32

    PubMed  CAS  Google Scholar 

  • Babiloni C, Visser PJ, Frisoni G, De Deyn PP, Bresciani L, Jelic V, Nagels G, Rodriguez G, Rossini PM, Vecchio F, Colombo D, Verhey F, Wahlund LO, Nobili F (2010) Cortical sources of resting EEG rhythms in mild cognitive impairment and subjective memory complaint. Neurobiol Aging 31:1787–1798

    PubMed  Google Scholar 

  • Babiloni C, Vecchio F, Lizio R, Ferri R, Rodriguez G, Marzano N, Frisoni GB, Rossini PM (2011) Resting state cortical rhythms in mild cognitive impairment and Alzheimer’s disease: electroencephalographic evidence. J Alzheimers Dis 26:201–214

    PubMed  Google Scholar 

  • Başar E, Başar-Eroglu C, Röschke J (1988) Do coherent patterns of strange attractor EEG reflect deterministic sensory-cognitive states of brain? In: Markus M, Muller M, Nicolis G (eds) From chemical to biological organization. Springer, Berlin, pp 297–306

    Google Scholar 

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

    PubMed  Google Scholar 

  • Bastiaansen M, Hagoort P (2003) Event-induced theta responses as a window on the dynamics of memory. Cortex 39:967–992 (review)

    PubMed  Google Scholar 

  • Belleville S, Chertkow H, Gauthier S (2007) Working memory and control of attention in persons with Alzheimer’s disease and mild cognitive impairment. Neuropsychology 21:458–469

    PubMed  Google Scholar 

  • Bendixen A, Schröger E, Winkler I (2009) I heard that coming: event-related potential evidence for stimulus-driven prediction in the auditory system. J Neurosci 29:8447–8451

    PubMed  CAS  Google Scholar 

  • Blankenship AB (1938) Memory span: a review of the literature. Psychol Bull 35:1–25

    Google Scholar 

  • Bocková M, Chládek J, Jurák P, Halámek J, Rektor I (2007) Executive functions processed in the frontal and lateral temporal cortices: intracerebral study. Clin Neurophysiol 118:2625–2636

    PubMed  Google Scholar 

  • Burgess AP, Gruzelier JH (1996) The reliability of event-related desynchronisation: a generalisability study analysis. Int J Psychophysiol 23:163–169

    PubMed  CAS  Google Scholar 

  • Burgess AP, Gruzelier JH (2000) Short duration power changes in the EEG during recognition memory for words and faces. Psychophysiology 37:596–606

    PubMed  CAS  Google Scholar 

  • Cabeza R (2002) Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychol Aging 17:85–100 (review)

    PubMed  Google Scholar 

  • Cantero JL, Atienza M, Stickgold R, Kahana MJ, Madsen JR, Kocsis B (2003) Sleep-dependent theta oscillations in the human hippocampus and neocortex. J Neurosci 23:10897–10903

    PubMed  CAS  Google Scholar 

  • Capotosto P, Perrucci MG, Brunetti M, Del Gratta C, Doppelmayr M, Grabner RH, Klimesch W, Neubauer A, Neuper C, Pfurtscheller G, Romani GL, Babiloni C (2009) Is there “neural efficiency” during the processing of visuo-spatial information in male humans? An EEG study. Behav Brain Res 205:468–474

    PubMed  Google Scholar 

  • Carter SF, Caine D, Burns A, Herholz K, Lambon Ralph MA (2012) Staging of the cognitive decline in Alzheimer’s disease: insights from a detailed neuropsychological investigation of mild cognitive impairment and mild Alzheimer’s disease. Int J Geriatr Psychiatry 27:423–432

    PubMed  Google Scholar 

  • Coull J, Nobre A (2008) Dissociating explicit timing from temporal expectation with fMRI. Curr Opin Neurobiol 18:137–144

    PubMed  CAS  Google Scholar 

  • de Araújo DB, Baffa O, Wakai RT (2002) Theta oscillations and human navigation: a magnetoencephalography study. J Cogn Neurosci 14:70–78

    PubMed  Google Scholar 

  • Deiber MP, Missonnier P, Bertrand O, Gold G, Fazio-Costa L, Ibañez V, Giannakopoulos P (2007) Distinction between perceptual and attentional processing in working memory tasks: a study of phase-locked and induced oscillatory brain dynamics. J Cogn Neurosci 19:158–172

    PubMed  Google Scholar 

  • Deiber MP, Ibañez V, Missonnier P, Herrmann F, Fazio-Costa L, Gold G, Giannakopoulos P (2009) Abnormal-induced theta activity supports early directed-attention network deficits in progressive MCI. Neurobiol Aging 30:1444–1452

    PubMed  Google Scholar 

  • Dien J, Spencer KM, Donchin E (2003) Localization of the event-related potential novelty response as defined by principal components analysis. Brain Res Cogn Brain Res 17:637–650

    PubMed  Google Scholar 

  • Doherty JR, Rao A, Mesulam MM, Nobre AC (2005) Synergistic effect of combined temporal and spatial expectations on visual attention. J Neurosci 25:8259–8266

    PubMed  CAS  Google Scholar 

  • Drzezga A, Becker JA, Van Dijk KR, Sreenivasan A, Talukdar T, Sullivan C, Schultz AP, Sepulcre J, Putcha D, Greve D, Johnson KA, Sperling RA (2011) Neuronal dysfunction and disconnection of cortical hubs in non-demented subjects with elevated amyloid burden. Brain 134:1635–1646

    PubMed  Google Scholar 

  • Engel AK, Fries P, Singer W (2001) Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci 2:704–716 (review)

    PubMed  CAS  Google Scholar 

  • Folstein M, Folstein S, McHugh P (1975) “Mini Mental State”—a practical method for grading the cognitive state of patients for the clinician. J Psychiatric Res 12:189–198

    CAS  Google Scholar 

  • Gasser T, Bacher P, Mocks J (1982) Transformations towards the normal distribution of broad band spectral parameters of the EEG. Electroencephalogr Clin Neurophysiol 53:119–124

    PubMed  CAS  Google Scholar 

  • Gevins A, Smith ME (2000) Neurophysiological measures of working memory and individual differences in cognitive ability and cognitive style. Cereb Cortex 10:829–839

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Gevins A, Smith ME, Leong H, McEvoy L, Whitfield S, Du R, Rush G (1998) Monitoring working memory load during computer-based tasks with EEG pattern recognition methods. Hum Factors 40:79–91

    PubMed  CAS  Google Scholar 

  • Giovagnoli AR, Del Pesce M, Mascheroni S, Simoncelli M, Laiacona M, Capitani E (1996) Trail making test: normative values from 287 normal adult controls. Ital J Neurol Sci 17:305–309

    PubMed  CAS  Google Scholar 

  • Grady CL, McIntosh AR, Horwitz B, Rapoport SI (2000) Age-related changes in the neural correlates of degraded and nondegraded face processing. Cogn Neuropsychol 17:165–186

    PubMed  CAS  Google Scholar 

  • Griesmayr B, Gruber WR, Klimesch W, Sauseng P (2010) Human frontal midline theta and its synchronization to gamma during a verbal delayed match to sample task. Neurobiol Learn Mem 93:208–215

    PubMed  Google Scholar 

  • Grunwald M, Weiss T, Krause W, Beyer L, Rost R, Gutberlet I, Gertz HJ (1999) Power of theta waves in the EEG of human subjects increases during recall of haptic information. Neurosci Lett 260:189–192

    PubMed  CAS  Google Scholar 

  • Hachinski VC, Iliff LD, Zilhka E, Du Boulay GH, McAllister VL, Marshall J, Russell RW, Symon L (1975) Cerebral blood flow in dementia. Arch Neurol 32:632–637

    PubMed  CAS  Google Scholar 

  • Hensel A, Riedel-Heller SG (2008) Measuring cognitive change in patients with suspected dementia-change norms are lacking for psychometric instruments Psychiatr Prax. 35:251–254

    Google Scholar 

  • Hughes CP, Berg L, Danziger WL, Coben LA, Martin RL (1982) A new clinical scale for the staging of dementia. Br J Psychiatry 140:566–572

    PubMed  CAS  Google Scholar 

  • Hutchinson S, Kobayashi M, Horkan CM, Pascual-Leone A, Alexander MP, Schlaug G (2002) Age-related differences in movement representation. Neuroimage 17:1720–1728

    PubMed  CAS  Google Scholar 

  • Ishii R, Shinosaki K, Ukai S, Inouye T, Ishihara T, Yoshimine T, Hirabuki N, Asada H, Kihara T, Robinson SE, Takeda M (1999) Medial prefrontal cortex generates frontal midline theta rhythm. NeuroReport 10:675–679

    PubMed  CAS  Google Scholar 

  • Jelic V, Johansson SE, Almkvist O, Shigeta M, Julin P, Nordberg A, Winblad B, Wahlund LO (2000) Quantitative electroencephalography in mild cognitive impairment: longitudinal changes and possible prediction of Alzheimer’s disease. Neurobiol Aging 21:533–540

    PubMed  CAS  Google Scholar 

  • Jensen O, Tesche CD (2002) Frontal theta activity in humans increases with memory load in a working memory task. Eur J Neurosci 15:1395–1399

    PubMed  Google Scholar 

  • Jeong J (2004) EEG dynamics in patients with Alzheimer’s disease. Clin Neurophysiol 115:1490–1505 (review)

    PubMed  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

    PubMed  CAS  Google Scholar 

  • Katz S, Ford AB, Moskowitz RW, Jackson BA, Jaffe MW (1963) Studies of illness in the aged. The index of ADL: a standardized measure of biological and psychosocial function. JAMA 185:914–919

    PubMed  CAS  Google Scholar 

  • Kim YH, Gitelman DR, Nobre AC, Parrish TB, LaBar KS, Mesulam MM (1999) The large-scale neural network for spatial attention displays multifunctional overlap but differential asymmetry. Neuroimage 9:269–277

    PubMed  CAS  Google Scholar 

  • Klimesch W (1996) Memory processes, brain oscillations and EEG synchronization. Int J Psychophysiol 24:61–100 (review)

    PubMed  CAS  Google Scholar 

  • Klimesch W (1997) EEG-alpha rhythms and memory processes. Int J Psychophysiol 26:319–340 (review)

    PubMed  CAS  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 (review)

    PubMed  CAS  Google Scholar 

  • Klimesch W, Schimke H, Pfurtscheller G (1993) Alpha frequency, cognitive load and memory performance. Brain Topogr 5:241–251

    PubMed  CAS  Google Scholar 

  • Klimesch W, Schimke H, Schwaiger J (1994) Episodic and semantic memory: an analysis in the EEG theta and alpha band. Electroencephalogr Clin Neurophysiol 91:428–441

    PubMed  CAS  Google Scholar 

  • Klimesch W, Doppelmayr M, Pachinger T, Russegger H (1997) Event-related desynchronization in the alpha band and the processing of semantic information. Brain Res Cogn Brain Res 6:83–94

    PubMed  CAS  Google Scholar 

  • Klimesch W, Russegger H, Doppelmayr M, Pachinger T (1998) A method for the calculation of induced band power: implications for the significance of brain oscillations. Electroencephalogr Clin Neurophysiol 108:123–130

    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

    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

    PubMed  CAS  Google Scholar 

  • Klimesch W, Hanslmayr S, Sauseng P, Gruber W, Brozinsky CJ, Kroll NE, Yonelinas AP, Doppelmayr M (2006) Oscillatory EEG correlates of episodic trace decay. Cereb Cortex 16:280–290

    PubMed  CAS  Google Scholar 

  • Krause CM (2006) Cognition- and memory-related ERD/ERS responses in the auditory stimulus modality. Prog Brain Res 159:197–207

    PubMed  Google Scholar 

  • Krause CM, Salminen PA, Sillanmäki L, Holopainen IE (2001) Event-related desynchronization and synchronization during a memory task in children. Clin Neurophysiol 112:2233–2240

    PubMed  CAS  Google Scholar 

  • Kubota Y, Sato W, Toichi M, Murai T, Okada T, Hayashi A, Sengoku A (2001) Frontal midline theta rhythm is correlated with cardiac autonomic activities during the performance of an attention demanding meditation procedure. Brain Res Cogn Brain Res 11:281–287

    PubMed  CAS  Google Scholar 

  • Kujala T, Tervaniemi M, Schröger E (2007) The mismatch negativity in cognitive and clinical neuroscience: theoretical and methodological considerations. Biol Psychol 74:1–19 (review)

    PubMed  Google Scholar 

  • Kveraga K, Ghuman AS, Bar M (2007) Top-down predictions in the cognitive brain. Brain Cogn 65:145–168

    PubMed  Google Scholar 

  • Kwak YT (2006) Quantitative EEG findings in different stages of Alzheimer’s disease. J Clin Neurophysiol 23:456–461

    PubMed  Google Scholar 

  • Lawton MP, Brody EM (1969) Assessment of older people: self-maintaining and instrumental activities of daily living. Gerontologist 9:179–186

    PubMed  CAS  Google Scholar 

  • Luck T, Busse A, Hensel A, Angermeyer MC, Riedel-Heller SG (2008) Mild cognitive impairment and development of dementia. Psychiatr Prax 35:331–336

    PubMed  Google Scholar 

  • Maguire EA, Frith CD (2003) Lateral asymmetry in the hippocampal response to the remoteness of autobiographical memories. J Neurosci 23:5302–5307

    PubMed  CAS  Google Scholar 

  • Makeig S, Delorme A, Westerfield M, Jung TP, Townsend J, Courchesne E, Sejnowski TJ (2004) Electroencephalographic brain dynamics following manually responded visual targets. PLoS Biol 2:e176

    PubMed  Google Scholar 

  • Maltseva I, Geissler HG, Başar E (2000) Alpha oscillations as an indicator of dynamic memory operations—anticipation of omitted stimuli. Int J Psychophysiol 36:185–197

    PubMed  CAS  Google Scholar 

  • Mattay VS, Fera F, Tessitore A, Hariri AR, Das S, Callicott JH, Weinberger DR (2002) Neurophysiological correlates of age-related changes in human motor function. Neurology 58:630–635

    PubMed  CAS  Google Scholar 

  • Mecklinger A, Kramer AF, Strayer DL (1992) Event related potentials and EEG components in a semantic memory search task. Psychophysiology 29:104–119

    PubMed  CAS  Google Scholar 

  • Mesulam MM (1998) From sensation to cognition. Brain 121:1013–1052

    PubMed  Google Scholar 

  • Metherate R, Cox CL, Ashe JH (1992) Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. J Neurosci 12:4701–4711

    PubMed  CAS  Google Scholar 

  • Missonnier P, Gold G, Herrmann FR, Fazio-Costa L, Michel JP, Deiber MP, Michon A, Giannakopoulos P (2006) Decreased theta event-related synchronization during working memory activation is associated with progressive mild cognitive impairment. Dement Geriatr Cogn Disord 22:250–259

    PubMed  Google Scholar 

  • Moretti DV, Miniussi C, Frisoni GB, Geroldi C, Zanetti O, Binetti G, Rossini PM (2007) Hippocampal atrophy and EEG markers in subjects with mild cognitive impairment. Clin Neurophysiol 118:2716–2729

    PubMed  CAS  Google Scholar 

  • Moretti DV, Frisoni GB, Binetti G, Zanetti O (2011) Anatomical substrate and scalp EEG markers are correlated in subjects with cognitive impairment and Alzheimer’s disease. Front Psychiatry 1:152

    PubMed  Google Scholar 

  • Näätänen R, Gaillard AW, Mäntysalo S (1978) Early selective-attention effect on evoked potential reinterpreted. Acta Psychol (Amst) 42:313–329

    Google Scholar 

  • Näätänen R, Paavilainen P, Rinne T, Alho K (2007) The mismatch negativity (MMN) in basic research of central auditory processing: a review. Clin Neurophysiol 118:2544–2590

    PubMed  Google Scholar 

  • Neuper C, Grabner RH, Fink A, Neubauer AC (2005) Long-term stability and consistency of EEG event-related (de-)synchronization across different cognitive tasks. Clin Neurophysiol 116:1681–1694

    PubMed  Google Scholar 

  • Nielson KA, Langenecker SA, Garavan H (2002) Differences in the functional neuroanatomy of inhibitory control across the adult life span. Psychol Aging 17:56–71

    PubMed  Google Scholar 

  • Nyenhuis DL, Garron DC (1997) Psychometric considerations when measuring cognitive decline in Alzheimer’s disease. Neuroepidemiology 16:185–190

    PubMed  CAS  Google Scholar 

  • O’Reilly JX, McCarthy KJ, Capizzi M, Nobre AC (2008) Acquisition of the temporal and ordinal structure of movement sequences in incidental learning. J Neurophysiol 99:2731–2735

    PubMed  Google Scholar 

  • Olichney JM, Morris SK, Ochoa C, Salmon DP, Thal LJ, Kutas M, Iragui VJ (2002) Abnormal verbal event related potentials in mild cognitive impairment and incipient Alzheimer’s disease. J Neurol Neurosurg Psychiatry 73:377–384

    PubMed  CAS  Google Scholar 

  • Pfurtscheller G, Lopes da Silva FH (1999) Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol 110:1842–1857

    PubMed  CAS  Google Scholar 

  • Pfurtscheller G, Neuper C, Mohl W (1994) Event-related desynchronization (ERD) during visual processing. Int J Psychophysiol 16:147–153

    PubMed  CAS  Google Scholar 

  • Polich J (1987) Response mode and P300 from auditory stimuli. Biol Psychol 25:61–71

    PubMed  CAS  Google Scholar 

  • Prichep LS, John ER, Ferris SH, Rausch L, Fang Z, Cancro R, Torossian C, Reisberg B (2006) Prediction of longitudinal cognitive decline in normal elderly with subjective complaints using electrophysiological imaging. Neurobiol Aging 27:471–481

    PubMed  CAS  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 

  • Raij T, McEvoy L, Mäkelä JP, Hari R (1997) Human auditory cortex is activated by omissions of auditory stimuli. Brain Res 745:134–143

    PubMed  CAS  Google Scholar 

  • Rey A (1958) L’Examen Clinique en Psychologie. Press Universitaire de France, Paris

  • Roh JH, Park MH, Ko D, Park KW, Lee DH, Han C, Jo SA, Yang KS, Jung KY (2011) Region and frequency specific changes of spectral power in Alzheimer’s disease and mild cognitive impairment. Clin Neurophysiol 122:2169–2176

    PubMed  Google Scholar 

  • Schimke H, Klimesch W, Pfurtscheller G (1990) Event-related desynchronization and the selection of an alpha-frequency band for quantifying cortical pre- and poststimulus activation. EEG EMG Z Elektroenzephalogr Elektromyogr Verwandte 21:219–225

    CAS  Google Scholar 

  • Shulman KI, Shedletsky R, Silver IL (1986) The challenge of time: clock-drawing and cognitive function in the elderly. Int J Geriatr Psychiatry 1:135–140

    Google Scholar 

  • Spehlmann R, Norcross K (1982) Cholinergic mechanisms in the production of focal cortical slow waves. Experientia 38:109–111

    PubMed  CAS  Google Scholar 

  • Stipacek A, Grabner RH, Neuper C, Fink A, Neubauer AC (2003) Sensitivity of human EEG alpha band desynchronization to different working memory components and increasing levels of memory load. Neurosci Lett 353:193–196

    PubMed  CAS  Google Scholar 

  • Swets JA (1998) Measuring the accuracy of diagnostic systems. Science 240:1285–1293

    Google Scholar 

  • Tales A, Haworth J, Nelson S, Snowden R, Wilcock G (2005a) Abnormal visual search in mild cognitive impairment and Alzheimer’s disease. Neurocase 11:80–84

    PubMed  Google Scholar 

  • Tales A, Snowden R, Haworth J, Wilcock G (2005b) Abnormal spatial and non-spatial cueing effects in mild cognitive impairment and Alzheimer’s disease. Neurocase 11:85–92

    PubMed  Google Scholar 

  • Tales A, Bayer AJ, Haworth J, Snowden RJ, Philips M, Wilcock G (2011) Visual search in mild cognitive impairment: a longitudinal study. J Alzheimer’s Dis 24:151–160

    Google Scholar 

  • Tesche CD, Karhu J (2000) Theta oscillations index human hippocampal activation during a working memory task. Proc Natl Acad Sci USA 97:919–924

    PubMed  CAS  Google Scholar 

  • van der Hiele K, Vein AA, Kramer CG, Reijntjes RH, van Buchem MA, Westendorp RG, Bollen EL, van Dijk JG, Middelkoop HA (2007) Memory activation enhances EEG abnormality in mild cognitive impairment. Neurobiol Aging 28:85–90

    PubMed  Google Scholar 

  • van Marwijk HWJ, Wallace P, De Bock GH, Hernans JO, Kptein AA, Mulder JD (1995) Evaluation of the feasibility, reliability and diagnostic value of shortened versions of the geriatric depression scale. Br J Gen Pract 45:195–199

    PubMed  Google Scholar 

  • Vannini P, Almkvist O, Dierks T, Lehmann C, Wahlund LO (2007) Reduced neuronal efficacy in progressive mild cognitive impairment: a prospective fMRI study on visuospatial processing. Psychiatry Res 156:43–57

    PubMed  Google Scholar 

  • Villa AE, Tetko IV, Dutoit P, Vantini G (2000) Non-linear cortico–cortical interactions modulated by cholinergic afferences from the rat basal forebrain. Biosystems 58:219–228

    PubMed  CAS  Google Scholar 

  • Zhuang P, Toro C, Grafman J, Manganotti P, Leocani L, Hallett M (1997) Event-related desynchronization (ERD) in the alpha frequency during development of implicit and explicit learning. Electroencephalogr Clin Neurophysiol 102:374–381

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Unità Operativa di Neurologia, Az. Ospedaliera “Cannizzaro”, Via Messina, 829, 95126, Catania, Italy

    Giuseppe Caravaglios, Emma Gabriella Muscoso, Giulia Di Maria & Erminio Costanzo

Authors
  1. Giuseppe Caravaglios
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emma Gabriella Muscoso
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Giulia Di Maria
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Erminio Costanzo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Giuseppe Caravaglios.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Caravaglios, G., Muscoso, E.G., Di Maria, G. et al. Theta responses are abnormal in mild cognitive impairment: evidence from analysis of theta event-related synchronization during a temporal expectancy task. J Neural Transm 120, 1093–1107 (2013). https://doi.org/10.1007/s00702-012-0921-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00702-012-0921-9

Keywords

Search

Navigation