Skip to main content
SpringerLink
Log in

Cholinergic modulation of auditory processing, sensory gating and novelty detection in human participants

  • Original Investigation
  • Published:
Psychopharmacology Aims and scope Submit manuscript

Abstract

Rationale

Suppression of redundant auditory information and facilitation of deviant, novel, or salient sounds can be assessed with paired-click and oddball tasks, respectively. Electrophysiological correlates of perturbed auditory processing found in these paradigms are likely to be a trait marker or candidate endophenotype for schizophrenia.

Objective

This is the first study to investigate the effects of the muscarinic M1 antagonist biperiden and the cholinesterase inhibitor rivastigmine on auditory-evoked potentials (AEPs), sensory gating, and mismatch negativity (MMN) in young, healthy volunteers.

Results

Biperiden increased P50 amplitude and prolonged N100 and P200 latency in the paired-click task but did not affect sensory gating. Rivastigmine was able to reverse the effects of biperiden on N100 and P200 latency. Biperiden increased P50 latency in the novelty oddball task, which was reversed by concurrent administration of rivastigmine. Rivastigmine shortened N100 latency and enhanced P3a amplitude in the novelty oddball paradigm, both of which were reversed by biperiden.

Conclusion

The muscarinic M1 receptor appears to be involved in preattentive processing of auditory information in the paired-click task. Additional effects of biperiden versus rivastigmine were reversed by a combination treatment, which renders attribution of these findings to muscarinic M1 versus muscarinic M2–M5 or nicotinic receptors much more difficult. It remains to be seen whether the effects of cholinergic drugs on AEPs are specifically related to the abnormalities found in schizophrenia. Alternatively, aberrant auditory processing could also be indicative of a general disturbance in neural functioning shared by several neuropsychiatric disorders and/or neurodegenerative changes seen in aging.

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
Fig. 6
Fig. 7

Similar content being viewed by others

Notes

  1. The existing literature on P300 abnormalities in schizophrenia has focused mostly on the P3b subcomponent, although a limited number of studies have also reported reduced P3a amplitudes (Grillon et al. 1990; Turetsky et al. 2000).

References

  • Adler LE, Pachtman E, Franks RD, Pecevich M, Waldo MC, Freedman R (1982) Neurophysiological evidence for a defect in neuronal mechanisms involved in sensory gating in schizophrenia. Biol Psychiatry 17:639–654

    PubMed  CAS  Google Scholar 

  • Adler LE, Olincy A, Waldo M, Harris JG, Griffith J, Stevens K, Flach K, Nagamoto H, Bickford P, Leonard S, Freedman R (1998) Schizophrenia, sensory gating, and nicotinic receptors. Schizophrenia Bull 24:189–202

    Article  CAS  Google Scholar 

  • Ally BA, Jones GE, Cole JA, Budson AE (2006) Sensory gating in patients with Alzheimer's disease and their biological children. Am J Alzheimers Dis Other Demen 21:439–447

    Article  PubMed  Google Scholar 

  • Amenedo E, Diaz F (1998) Aging-related changes in processing of non-target and target stimuli during an auditory oddball task. Biol Psychol 48:235–267

    Article  PubMed  CAS  Google Scholar 

  • Anderer P, Semlitsch HV, Saletu B (1996) Multichannel auditory event-related brain potentials: effects of normal aging on the scalp distribution of N1, P2, N2 and P300 latencies and amplitudes. Electroencephalogr Clin Neurophysiol 99:458–472

    Article  PubMed  CAS  Google Scholar 

  • Anderer P, Saletu B, Semlitsch HV, Pascual-Marqui RD (2003) Non-invasive localization of P300 sources in normal aging and age-associated memory impairment. Neurobiol Aging 24:463–479

    Article  PubMed  CAS  Google Scholar 

  • Baldeweg T, Klugman A, Gruzelier J, Hirsch SR (2004) Mismatch negativity potentials and cognitive impairment in schizophrenia. Schizophr Res 69:203–217

    Article  PubMed  Google Scholar 

  • Bolden C, Cusack B, Richelson E (1992) Antagonism by antimuscarinic and neuroleptic compounds at the five cloned human muscarinic cholinergic receptors expressed in Chinese hamster ovary cells. J Pharmacol Exp Ther 260:576–580

    PubMed  CAS  Google Scholar 

  • Bond A, Lader M (1974) The use of analogue scales in rating subjective feelings. Brit J Med Psychol 80:1–46

    Google Scholar 

  • Bora E, Veznedaroglu B, Kayahan B (2005) The effect of galantamine added to clozapine on cognition of five patients with schizophrenia. Clin Neuropharmacol 28:139–141

    Article  PubMed  Google Scholar 

  • Boutros N, Torello MW, Burns EM, Wu SS, Nasrallah HA (1995) Evoked potentials in subjects at risk for Alzheimer's disease. Psychiatry Res 57:57–63

    Article  PubMed  CAS  Google Scholar 

  • Boutros NN, Korzyukov O, Jansen B, Feingold A, Bell M (2004) Sensory gating deficits during the mid-latency phase of information processing in medicated schizophrenia patients. Psychiatry Res 126:203–215

    Article  PubMed  Google Scholar 

  • Boutros NN, Brockhaus-Dumke A, Gjini K, Vedeniapin A, Elfakhani M, Burroughs S, Keshavan M (2009) Sensory-gating deficit of the N100 mid-latency auditory evoked potential in medicated schizophrenia patients. Schizophr Res 113:339–346

    Article  PubMed  Google Scholar 

  • Bramon E, Croft RJ, McDonald C, Virdi GK, Gruzelier JG, Baldeweg T, Sham PC, Frangou S, Murray RM (2004a) Mismatch negativity in schizophrenia: a family study. Schizophr Res 67:1–10

    Article  PubMed  Google Scholar 

  • Bramon E, Rabe-Hesketh S, Sham P, Murray RM, Frangou S (2004b) Meta-analysis of the P300 and P50 waveforms in schizophrenia. Schizophr Res 70:315–329

    Article  PubMed  Google Scholar 

  • Brockhaus-Dumke A, Schultze-Lutter F, Mueller R, Tendolkar I, Bechdolf A, Pukrop R, Klosterkoetter J, Ruhrmann S (2008) Sensory gating in schizophrenia: P50 and N100 gating in antipsychotic-free subjects at risk, first-episode, and chronic patients. Biol Psychiatry 64:376–384

    Article  PubMed  Google Scholar 

  • Buchanan RW, Summerfelt A, Tek C, Gold J (2002) An open-label trial of adjunctive donepezil for cognitive impairments in patients with schizophrenia. Schizophr Res 59:29–33

    Article  Google Scholar 

  • Buchanan RW, Conley RR, Dickinson D, Ball MP, Feldman S, Gold JM, McMahon RP (2008) Galantamine for the treatment of cognitive impairments in people with schizophrenia. Am J Psychiatry 165:82–89

    Article  PubMed  Google Scholar 

  • Buchwald JS, Rubinstein EH, Schwafel J, Strandburg RJ (1991) Midlatency auditory evoked responses: differential effects of a cholinergic agonist and antagonist. Electroencephalogr Clin Neurophysiol 80:303–309

    Article  PubMed  CAS  Google Scholar 

  • Cancelli I, Cadore IP, Merlino G, Valentinis L, Moratti U, Bergonzi P, Gigli GL, Valente M (2006) Sensory gating deficit assessed by P50/Pb middle latency event related potential in Alzheimer's disease. J Clin Neurophysiol 23:421–425

    Article  PubMed  Google Scholar 

  • Clementz BA, Blumenfeld LD (2001) Multichannel electroencephalographic assessment of auditory evoked response suppression in schizophrenia. Exp Brain Res 139:377–390

    Article  PubMed  CAS  Google Scholar 

  • Comerchero MD, Polich J (1999) P3a and P3b from typical auditory and visual stimuli. Clin Neurophysiol 110:24–30

    Article  PubMed  CAS  Google Scholar 

  • Curran HV, Pooviboonsuk P, Dalton JA, Lader MH (1998) Differentiating the effects of centrally acting drugs on arousal and memory: an event-related potential study of scopolamine, lorazepam and diphenhydramine. Psychopharmacology 135:27–36

    Article  PubMed  CAS  Google Scholar 

  • Donchin E (1981) Surprise!…Surprise? Psychophysiology 18:493–513

    Article  PubMed  CAS  Google Scholar 

  • Dyer MA, Freudenreich O, Culhane MA, Pachas GN, Deckersbach T, Murphy E, Goff DC, Evins AE (2008) High-dose galantamine augmentation inferior to placebo on attention, inhibitory control and working memory performance in nonsmokers with schizophrenia. Schizophr Res 102:88–95

    Article  PubMed  Google Scholar 

  • Erwin RJ, Turetsky BI, Moberg P, Gur RC, Gur RE (1998) P50 abnormalities in schizophrenia: relationship to clinical and neuropsychological indices of attention. Schizophr Res 33:157–167

    Article  PubMed  CAS  Google Scholar 

  • Farlow MR (2003) Update on rivastigmine. Neurologist 9:230–234

    Article  PubMed  Google Scholar 

  • Fein G, Biggins C, Van Dyke C (1994) The auditory P50 response is normal in Alzheimer's disease when measured via a paired click paradigm. Electroencephalogr Clin Neurophysiol 92:536–545

    Article  PubMed  CAS  Google Scholar 

  • Fjell AM, Walhovd KB (2004) Life-span changes in P3a. Psychophysiology 41:575–583

    Article  PubMed  Google Scholar 

  • Fjell AM, Walhovd KB, Fischl B, Reinvang I (2007) Cognitive function, P3a/P3b brain potentials, and cortical thickness in aging. Hum Brain Mapp 28:1098–1116

    Article  PubMed  Google Scholar 

  • Ford JM (1999) Schizophrenia: the broken P300 and beyond. Psychophysiology 36:667–682

    Article  PubMed  CAS  Google Scholar 

  • Ford JM, Pfefferbaum A (1991) Event-related potentials and eyeblink responses in automatic and controlled processing: effects of age. Electroencephalogr Clin Neurophysiol 78:361–377

    Article  PubMed  CAS  Google Scholar 

  • Friedman JI (2004) Cholinergic targets for cognitive enhancement in schizophrenia: focus on cholinesterase inhibitors and muscarinic agonists. Psychopharmacology 174:45–53

    Article  PubMed  CAS  Google Scholar 

  • Friedman JI, Adler DN, Howanitz E, Harvey PD, Brenner G, Temporini H, White L, Parrella M, Davis KL (2002) A double blind placebo controlled trial of donepezil adjunctive treatment to risperidone for the cognitive impairment of schizophrenia. Biol Psychiatry 51:349–357

    Article  PubMed  CAS  Google Scholar 

  • Furey ML, Drevets WC (2006) Antidepressant efficacy of the antimuscarinic drug scopolamine: a randomized, placebo-controlled clinical trial. Arch Gen Psychiatry 63:1121–1129

    Article  PubMed  CAS  Google Scholar 

  • Furey ML, Khanna A, Hoffman EM, Drevets WC (2010) Scopolamine produces larger antidepressant and antianxiety effects in women than in men. Neuropsychopharmacol 35:2479–2488

    Article  CAS  Google Scholar 

  • Garrido MI, Kilner JM, Stephan KE, Friston KJ (2009) The mismatch negativity: a review of underlying mechanisms. Clin Neurophysiol 120:453–463

    Article  PubMed  Google Scholar 

  • Gjini K, Arfken C, Boutros NN (2010) Relationships between sensory “gating out” and sensory “gating in” of auditory evoked potentials in schizophrenia: a pilot study. Schizophr Res 121:139–145

    Article  PubMed  Google Scholar 

  • Gmehlin D, Kreisel SH, Bachmann S, Weisbrod M, Thomas C (2011) Age effects on preattentive and early attentive auditory processing of redundant stimuli: is sensory gating affected by physiological aging? J Gerontol A Biol Sci Med Sci 66:1043–1053

    Article  PubMed  Google Scholar 

  • Golob EJ, Johnson JK, Starr A (2001a) Auditory event-related potentials during target detection are abnormal in mild cognitive impairment. Clin Neurophysiol 113:151–161

    Article  Google Scholar 

  • Golob EJ, Miranda GG, Johnson JK, Starr A (2001b) Sensory cortical interactions in aging, mild cognitive impairment, and Alzheimer's disease. Neurobiol Aging 22:755–763

    Article  PubMed  CAS  Google Scholar 

  • Golob EJ, Irimajiri R, Starr A (2007) Auditory cortical activity in amnestic mild cognitive impairment: relationship to subtype and conversion to dementia. Brain 130:740–752

    Article  PubMed  Google Scholar 

  • Grillon C, Courchesne E, Ameli R, Geyer MA, Braff DL (1990) Increased distractibility in schizophrenic patients. Electrophysiologic and behavioral evidence. Arch Gen Psychiatry 47:171–179

    Article  PubMed  CAS  Google Scholar 

  • Grunwald T, Boutros NN, Pezer N, von Oertzen J, Fernandez G, Schaller C, Elger CE (2003) Neuronal substrates of sensory gating within the human brain. Biol Psychiatry 53:511–519

    Article  PubMed  Google Scholar 

  • Hall MH, Schulze K, Bramon E, Murray RM, Sham P, Rijsdijk F (2006) Genetic overlap between P300, P50, and duration mismatch negativity. Am J Med Genet B Neuropsychiatr Genet 141B:336–343

    Article  PubMed  Google Scholar 

  • Hämäläinen M, Hari R, Ilmoniemi RJ, Knuutila J, Lounasmaa OV (1993) Magnetoencephalography—theory, instrumentation, and applications to noninvasive studies of the working human brain. Rev Mod Phys 65:413–497

    Article  Google Scholar 

  • Hollmann M, Brode E, Greger G, Müller-Peltzer H, Wetzelsberger N (1984) Biperiden effects and plasma levels in volunteers. Eur J Clin Pharmacol 27:619–621

    Article  PubMed  CAS  Google Scholar 

  • Hollmann M, Müller-Peltzer H, Greger G, Brode E, Perucca E, Grimaldi R, Crema A (1987) Pharmacokinetic–dynamic study on different oral biperiden formulations in volunteers. Pharmacopsychiatry 20:72–77

    Article  PubMed  CAS  Google Scholar 

  • Hong X, Chan RC, Zhuang X, Jiang T, Wan X, Wang J, Xiao B, Zhou H, Jiang L, Weng B (2009) Neuroleptic effects on P50 sensory gating in patients with first-episode never-medicated schizophrenia. Schizophr Res 108:151–157

    Article  PubMed  Google Scholar 

  • Inami R, Kirino E, Inoue R, Arai H (2005) Transdermal nicotine administration enhances automatic auditory processing reflected by mismatch negativity. Pharmacol Biochem Behav 80:453–461

    Article  PubMed  CAS  Google Scholar 

  • Iragui VJ, Kutas M, Mitchiner MR, Hillyard SA (1993) Effects of aging on event-related brain potentials and reaction times in an auditory oddball task. Psychophysiology 30:10–22

    Article  PubMed  CAS  Google Scholar 

  • Irimajiri R, Golob EJ, Starr A (2005) Auditory brain-stem, middle- and long-latency evoked potentials in mild cognitive impairment. Clin Neurophysiol 116:1918–1929

    Article  PubMed  CAS  Google Scholar 

  • Jann MW, Shirley KL, Small GW (2002) Clinical pharmacokinetics and pharmacodynamics of cholinesterase inhibitors. Clin Pharmacokinet 41:719–739

    Article  PubMed  CAS  Google Scholar 

  • Jasper H (1958) The ten-twenty electrode system of the international federation. Electroencephalogr Clin Neurophysiol 10:371–375

    Google Scholar 

  • Javitt DC, Spencer KM, Thaker GK, Winterer G, Hajós M (2008) Neurophysiological biomarkers for drug development in schizophrenia. Nat Rev Drug Discov 7:68–83

    Article  PubMed  CAS  Google Scholar 

  • Jeon YW, Polich J (2001) P300 asymmetry in schizophrenia: a meta-analysis. Psychiatry Res 104:61–74

    Article  PubMed  CAS  Google Scholar 

  • Jin Y, Potkin SG, Patterson JV, Sandman CA, Hetrick WP, Bunney WE Jr (1997) Effects of P50 temporal variability on sensory gating in schizophrenia. Psychiatry Res 70:71–81

    Article  PubMed  CAS  Google Scholar 

  • Jin Y, Bunney WE Jr, Sandman CA, Patterson JV, Fleming K, Moenter JR, Kalali AH, Hetrick WP, Potkin SG (1998) Is P50 suppression a measure of sensory gating in schizophrenia? Biol Psychiatry 43:873–878

    Article  PubMed  CAS  Google Scholar 

  • Johannesen JK, Kieffaber PD, O'Donnell BF, Shekhar A, Evans JD, Hetrick WP (2005) Contributions of subtype and spectral frequency analyses to the study of P50 ERP amplitude and suppression in schizophrenia. Schizophr Res 78:269–284

    Article  PubMed  Google Scholar 

  • Johnstone EC, Crow TJ, Ferrier IN, Frith CD, Owens DGC, Bourne RC, Gamble SJ (1983) Adverse effects of anticholinergic medication on positive schizophrenic symptoms. Psychol Med 13:513–527

    Article  PubMed  CAS  Google Scholar 

  • Juckel G, Clotz F, Frodl T, Kawohl W, Hampel H, Pogarell O, Hegerl U (2008) Diagnostic usefulness of cognitive auditory event-related p300 subcomponents in patients with Alzheimers disease? J Clin Neurophysiol 25:147–152

    Article  PubMed  Google Scholar 

  • Kadir A, Darreh-Shori T, Almkvist O, Wall A, Langstrom B, Nordberg A (2007) Changes in brain 11C-nicotine binding sites in patients with mild Alzheimer's disease following rivastigmine treatment as assessed by PET. Psychopharmacology 191:1005–1014

    Article  PubMed  CAS  Google Scholar 

  • Karoumi B, Laurent A, Rosenfeld F, Rochet T, Brunon AM, Dalery J, d’Amato T, Saoud M (2000) Alteration of event related potentials in siblings discordant for schizophrenia. Schizophr Res 41:325–334

    Article  PubMed  CAS  Google Scholar 

  • Katayama S, Ishizaki F, Yamamura Y, Khoriyama T, Kito S (1990) Effects of anticholinergic antiparkinsonian drugs on binding of muscarinic receptor subtypes in rat brain. Res Commun Chem Path 69:261–270

    CAS  Google Scholar 

  • Kisley MA, Olincy A, Robbins E, Polk SD, Adler LE, Waldo MC, Freedman R (2003) Sensory gating impairment associated with schizophrenia persists into REM sleep. Psychophysiology 40:29–38

    Article  PubMed  Google Scholar 

  • Kisley MA, Noecker TL, Guinther PM (2004) Comparison of sensory gating to mismatch negativity and self-reported perceptual phenomena in healthy adults. Psychophysiology 41:604–612

    Article  PubMed  Google Scholar 

  • Kisley MA, Davalos DB, Engleman LL, Guinther PM, Davis HP (2005) Age-related change in neural processing of time-dependent stimulus features. Cogn Brain Res 25:913–925

    Article  Google Scholar 

  • Knight RT (1987) Aging decreases auditory event-related potentials to unexpected stimuli in humans. Neurobiol Aging 8:109–113

    Article  PubMed  CAS  Google Scholar 

  • Laurent A, Garcia-Larrea L, d’Amato T, Bosson JL, Saoud M, Marie-Cardine M, Maugiere F, Dalery J (1999) Auditory event-related potentials and clinical scores in unmedicated schizophrenic patients. Psychiatry Res 86:229–238

    Article  PubMed  CAS  Google Scholar 

  • Lee BJ, Lee JG, Kim YH (2007) A 12-week, double-blind, placebo-controlled trial of donepezil as an adjunct to haloperidol for treating cognitive impairments in patients with chronic schizophrenia. J Psychopharmacol 21:421–427

    Article  PubMed  CAS  Google Scholar 

  • Lefevre G, Sedek G, Jhee SS, Leibowitz MT, Huang HL, Enz A, Maton S, Ereshefsky L, Pommier F, Schmidli H, Appel-Dingemanse S (2008) Pharmacokinetics and pharmacodynamics of the novel daily rivastigmine transdermal patch compared with twice-daily capsules in Alzheimer's disease patients. Clin Pharmacol Ther 83:106–114

    Article  PubMed  CAS  Google Scholar 

  • Leiser SC, Dunlop J, Bowlby MR, Devilbiss DM (2011) Aligning strategies for using EEG as a surrogate biomarker: a review of preclinical and clinical research. Biochem Pharmacol 81:1408–1421

    Article  PubMed  CAS  Google Scholar 

  • Light GA, Braff DL (2005) Mismatch negativity deficits are associated with poor functioning in schizophrenia patients. Arch Gen Psychiatry 62:127–136

    Article  PubMed  Google Scholar 

  • Lijffijt M, Lane SD, Meier SL, Boutros NN, Burroughs S, Steinberg JL, Moeller FG, Swann AC (2009) P50, N100 and P200 sensory gating: relationships with behavioral inhibition, attention, and working memory. Psychophysiology 46:1059–1068

    Article  PubMed  Google Scholar 

  • McGhie A, Chapman J (1961) Disorders of attention and perception in early schizophrenia. Br J Med Psychol 34:103–116

    Article  PubMed  CAS  Google Scholar 

  • McNair DM, Lorr M, Droppleman LF (1971) Manual for the profile of mood states. Educational and Industrial Testing Service, Educational and Industrial Testing Service

  • Meador KJ, Loring DW, Adams RJ, Patel BR, Davis HC, Hammond EJ (1987) Central cholinergic systems and the P3 evoked potential. Int J Neurosci 33:199–205

    Article  PubMed  CAS  Google Scholar 

  • Meador KJ, Loring DW, Lee GP, Taylor HS, Hughes DR, Feldman DS (1988) In vivo probe of central cholinergic systems. J Gerontol 43:M158–M162

    Article  PubMed  CAS  Google Scholar 

  • Meador KJ, Loring DW, Davis HC, Sethi KD, Patel BR, Adams RJ, Hammond EJ (1989) Cholinergic and serotonergic effects on the P3 potential and recent memory. J Clin Exp Neuropsychol 11:252–260

    Article  PubMed  CAS  Google Scholar 

  • Meador KJ, Loring DW, Hendrix N, Nichols ME, Oberzan R, Moore EE (1995) Synergistic anticholinergic and antiserotonergic effects in humans. J Clin Exp Neuropsychol 17:611–621

    Article  PubMed  CAS  Google Scholar 

  • Mintzer J, Burns A (2000) Anticholinergic side-effects of drugs in elderly people. J R Soc Med 93:457–462

    PubMed  CAS  Google Scholar 

  • Miranda MI, Ramirez-Lugo L, Bermudez-Rattoni F (2000) Cortical cholinergic activity is related to the novelty of the stimulus. Brain Res 882:230–235

    Article  PubMed  CAS  Google Scholar 

  • Näätänen R, Pakarinen S, Rinne T, Takegata R (2004) The mismatch negativity (MMN): towards the optimal paradigm. Clin Neurophysiol 115:140–144

    Article  PubMed  Google Scholar 

  • Nagamoto HT, Adler LE, Waldo MC, Freedman R (1989) Sensory gating in schizophrenics and normal controls: effects of changing stimulation interval. Biol Psychiatry 25:549–561

    Article  PubMed  CAS  Google Scholar 

  • Ogino S, Miyamoto S, Tenjin T, Kitajima R, Ojima K, Miyake N, Funamoto Y, Arai J, Tsukahara S, Ito Y, Tadokoro M, Anai K, Tatsunami S, Kubota H, Kaneda Y, Yamaguchi S (2011) Effects of discontinuation of long-term biperiden use on cognitive function and quality of life in schizophrenia. Prog Neuro-Psychopharmacol Biol Psychiatry 35:78–83

    Article  CAS  Google Scholar 

  • Olincy A, Braff DL, Adler LE, Cadenhead KS, Calkins ME, Dobie DJ, Green MF, Greenwood TA, Gur RE, Gur RC, Light GA, Mintz J, Nuechterlein KH, Radant AD, Schork NJ, Seidman LJ, Siever LJ, Silverman JM, Stone WS, Swerdlow NR, Tsuang DW, Tsuang MT, Turetsky BI, Wagner BD, Freedman R (2010) Inhibition of the P50 cerebral evoked response to repeated auditory stimuli: results from the Consortium on Genetics of Schizophrenia. Schizophr Res 119:175–182

    Article  PubMed  Google Scholar 

  • Onofrj M, Thomas A, Iacono D, Luciano AL, Di Iorio A (2003) The effects of a cholinesterase inhibitor are prominent in patients with fluctuating cognition: a part 3 study of the main mechanism of cholinesterase inhibitors in dementia. Clin Neuropharmacol 26:239–251

    Article  PubMed  CAS  Google Scholar 

  • Oranje B, Geyer MA, Bocker KBE, Kenemans JL, Verbaten MN (2006) Prepulse inhibition and P50 suppression: commonalities and dissociations. Psychiatry Res 143:147–158

    Article  PubMed  Google Scholar 

  • Patterson JV, Jin Y, Gierczak M, Hetrick WP, Potkin S, Bunney WE Jr, Sandman CA (2000) Effects of temporal variability on P50 and the gating ratio in schizophrenia: a frequency domain adaptive filter single-trial analysis. Arch Gen Psychiatry 57:57–64

    Article  PubMed  CAS  Google Scholar 

  • Pekkonen E, Jousmaki V, Partanen J, Karhu J (1993) Mismatch negativity area and age-related auditory memory. Electroencephalogr Clin Neurophysiol 87:321–325

    Article  PubMed  CAS  Google Scholar 

  • Pekkonen E, Jousmaki V, Kononen M, Reinikainen K, Partanen J (1994) Auditory sensory memory impairment in Alzheimer's disease: an event-related potential study. NeuroReport 5:2537–2540

    Article  PubMed  CAS  Google Scholar 

  • Pekkonen E, Hirvonen J, Jaaskelainen IP, Kaakkola S, Huttunen J (2001) Auditory sensory memory and the cholinergic system: implications for Alzheimer's disease. NeuroImage 14:376–382

    Article  PubMed  CAS  Google Scholar 

  • Pekkonen E, Jaaskelainen IP, Kaakkola S, Ahveninen J (2005) Cholinergic modulation of preattentive auditory processing in aging. NeuroImage 27:387–392

    Article  PubMed  Google Scholar 

  • Pontifex MB, Hillman CH, Polich J (2009) Age, physical fitness, and attention: P3a and P3b. Psychophysiology 46:379–387

    Article  PubMed  Google Scholar 

  • Potter DD, Pickles CD, Roberts RC, Rugg MD (2000) The effect of cholinergic receptor blockade by scopolamine on memory performance and the auditory P3. J Psychophysiol 14:11–23

    Article  Google Scholar 

  • Price GW, Michie PT, Johnston J, Innes-Brown H, Kent A, Clissa P et al (2006) A multivariate electrophysiological endophenotype, from a unitary cohort, shows greater research utility than any single feature in the Western Australian family study of schizophrenia. Biol Psychiatry 60:1–10

    Article  PubMed  Google Scholar 

  • Pritchard W, Sokhadze E, Houlihan M (2004) Effects of nicotine and smoking on event-related potentials: a review. Nicotine Tob Res 6:961–984

    Article  PubMed  CAS  Google Scholar 

  • Riekkinen P Jr, Paakkonen A, Karhu J, Partanen J, Soininen H, Laakso M, Riekkine P Sr (1997) THA disrupts mismatch negativity in Alzheimer disease. Psychopharmacology 133:203–206

    Article  PubMed  CAS  Google Scholar 

  • Rinne T, Alho K, Ilmoniemi RJ, Virtanen J, Naatanen R (2000) Separate time behaviors of the temporal and frontal mismatch negativity sources. NeuroImage 12:14–19

    Article  PubMed  CAS  Google Scholar 

  • Risch SC, Horner MD, McGurk SR, Palecko S, Markowitz JS, Nahas Z, DeVane CL (2007) Double-blind donepezil-placebo crossover augmentation study of atypical antipsychotics in chronic, stable schizophrenia: a pilot study. Schizophr Res 93:131–135

    Article  PubMed  Google Scholar 

  • Rosler M, Anand R, Cicin-Sain A, Gauthier S, Agid Y, Dal-Bianco P, Stahelin HB, Hartman R, Gharabawi M (1999) Efficacy and safety of rivastigmine in patients with Alzheimer's disease: international randomised controlled trial. BMJ 318:633–638

    Article  PubMed  CAS  Google Scholar 

  • Sarter M, Lustig C, Taylor SF (2012) Cholinergic contributions to the cognitive symptoms of schizophrenia and the viability of cholinergic treatments. Neuropharmacology 62:1544–1553

    Article  PubMed  CAS  Google Scholar 

  • Schiff S, Valenti P, Andrea P, Lot M, Bisiacchi P, Gatta A, Amodio P (2008) The effect of aging on auditory components of event-related brain potentials. Clin Neurophysiol 119:1795–1802

    Article  PubMed  Google Scholar 

  • Schubert MH, Young KA, Hicks PB (2006) Galantamine improves cognition in schizophrenic patients stabilized on risperidone. Biol Psychiatry 60:530–533

    Article  PubMed  CAS  Google Scholar 

  • Semlitsch HV, Anderer P, Schuster P, Presslich O (1986) A solution for reliable and valid reduction of ocular artifacts, applied to the P300 ERP. Psychophysiology 23:695–703

    Article  PubMed  CAS  Google Scholar 

  • Shekhar A, Potter WZ, Lightfoot J, Lienemann J, Dubé S, Mallinckrodt C, Bymaster FP, McKinzie DL, Felder CC (2008) Selective muscarinic receptor agonist xanomeline as a novel treatment approach for schizophrenia. Am J Psychiatry 165:1033–1039

    Article  PubMed  Google Scholar 

  • Simons CJP, Sambeth A, Krabbendam L, Pfeifer S, Van Os J, Riedel WJ (2011) Auditory P300 and N100 components as intermediate phenotypes for psychotic disorder: familial liability and reliability. Clin Neurophysiol 122:1984–1990

    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 

  • Tandon R, Mann NA, Eisner WH, Coppard N (1990) Effect of anticholinergic medication on positive and negative symptoms in medication-free schizophrenic patients. Psychiatry Res 31:235–241

    Article  PubMed  CAS  Google Scholar 

  • Tandon R, DeQuardo JR, Goodson J, Mann NA, Greden JF (1992) Effect of anticholinergics on positive and negative symptoms in schizophrenia. Psychopharmacol Bull 28:297–302

    PubMed  CAS  Google Scholar 

  • Thomas C, vom Berg I, Rupp A, Seidl U, Schroder J, Roesch-Ely D, Kreisel SH, Mundt C, Weisbrod M (2010) P50 gating deficit in Alzheimer dementia correlates to frontal neuropsychological function. Neurobiol Aging 31:416–424

    Article  PubMed  CAS  Google Scholar 

  • Turetsky BI, Cannon TD, Gur RE (2000) P300 subcomponent abnormalities in schizophrenia: III. Deficits in unaffected siblings of schizophrenic probands. Biol Psychiatry 47:380–390

    Article  PubMed  CAS  Google Scholar 

  • Turetsky BI, Bilker WB, Siegel SJ, Kohler CG, Gur RE (2009) Profile of auditory information-processing deficits in schizophrenia. Psychiatry Res 165:27–37

    Article  PubMed  Google Scholar 

  • Umbricht D, Krljes S (2005) Mismatch negativity in schizophrenia: a meta-analysis. Schizophr Res 76:1–23

    Article  PubMed  Google Scholar 

  • van der Stelt O, Lieberman JA, Belger A (2005) Auditory P300 in high-risk, recent-onset and chronic schizophrenia. Schizophr Res 77:309–320

    Article  PubMed  Google Scholar 

  • Wezenberg E, Verkes RJ, Sabbe BG, Ruigt GS, Hulstijn W (2005) Modulation of memory and visuospatial processes by biperiden and rivastigmine in elderly healthy subjects. Psychopharmacology 181:582–594

    Article  PubMed  CAS  Google Scholar 

  • Williams TJ, Nuechterlein KH, Subotnik KL, Yee CM (2011) Distinct neural generators of sensory gating in schizophrenia. Psychophysiology 48:470–478

    Article  PubMed  Google Scholar 

  • Zouridakis G, Boutros NN (1992) Stimulus parameter effects on the P50 evoked response. Biol Psychiatry 32:839–841

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Suzanne Holthuijsen, Karin Joanknecht, and Conny Quaedflieg for their assistance with the EEG recording.

Conflict of interest

The authors declare that, except for income received from their primary employer, no financial support or compensation has been received from any individual or corporate entity over the past three years for research or professional service. There are no personal financial holdings that could be perceived as constituting a potential conflict of interest. The authors have full control of all primary data and agree to allow the journal to review data if requested.

Author information

Authors and Affiliations

  1. Faculty of Psychology and Neuroscience, Department of Neuropsychology and Psychopharmacology, Maastricht University, P.O. Box 616, 6200, MD, Maastricht, The Netherlands

    Inge Klinkenberg, Arjan Blokland, Wim J. Riedel & Anke Sambeth

Authors
  1. Inge Klinkenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Arjan Blokland
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wim J. Riedel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anke Sambeth
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Inge Klinkenberg.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Klinkenberg, I., Blokland, A., Riedel, W.J. et al. Cholinergic modulation of auditory processing, sensory gating and novelty detection in human participants. Psychopharmacology 225, 903–921 (2013). https://doi.org/10.1007/s00213-012-2872-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-012-2872-0

Keywords

Search

Navigation