Abstract
Paired pulse suppression is an electrophysiological method used to evaluate sensory suppression and often applied to patients with psychiatric disorders. However, it remains unclear whether the suppression comes from specific inhibitory mechanisms, refractoriness, or fatigue. In the present study, to investigate mechanisms of suppression induced by an auditory paired pulse paradigm in 19 healthy subjects, magnetoencephalography was employed. The control stimulus was a train of 25-ms pure tones of 65 dB SPL for 2500 ms. In order to evoke a test response, the sound pressure of two consecutive tones at 2200 ms in the control sound was increased to 80 dB (Test stimulus). Similar sound pressure changes were also inserted at 1000 (CS2) and 1600 (CS1) ms as conditioning stimuli. Four stimulus conditions were used; (1) Test alone, (2) Test + CS1, (3) Test + CS1 + CS2, and (4) Test + CS2, with the four sound stimuli randomly presented and cortical responses averaged at least 100 times for each condition. The baseline-to-peak and peak-to-peak amplitudes of the P50m, N100m, and P200m components of the test response were compared among the four conditions. In addition, the response to CS1 was compared between conditions (2) and (3). The results showed significant test response suppression by CS1. While the response to CS1 was significantly suppressed when CS2 was present, it did not affect suppression of the test response by CS1. It was thus suggested that the amplitude of the response to a conditioning stimulus is not a factor to determine the inhibitory effects of the test response, indicating that suppression is due to an external influence on the excitatory pathway.
Similar content being viewed by others
Data Availability
The datasets generated during and analysed during the current study are available from the corresponding author on reasonable request.
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
Baker N, Adler LE, Franks RD, Waldo M, Berry S, Nagamoto H, Muckle A, Freedman R (1987) Neurophysiological assessment of sensory gating in psychiatric inpatients: comparison between schizophrenia and other diagnoses. Biol Psychiatry 22:603–617
Budd TW, Barry RJ, Gordon E, Rennie C, Michie PT (1998) Decrement of the N1 auditory event-related potential with stimulus repetition: habituation vs. refractoriness. Int J Psychophysiol 31:51–68
Cheng CH, Chan PS, Liu CY, Hsu SC (2016) Auditory sensory gating in patients with bipolar disorders: a meta-analysis. J Affect Disord 203:199–203
Chien YL, Hsieh MH, Gau SS (2019) P50–N100-P200 sensory gating deficits in adolescents and young adults with autism spectrum disorders. Prog Neuro-Psychopharmacol Biol Psychiatry 95:109683
Dalecki A, Johnstone SJ, Croft RJ (2015) Clarifying the functional process represented by P50 suppression. Int J Psychophysiol 96:149–154
Fruhstorfer H, Soveri P, Järvilehto T (1970) Short-term habituation of the auditory evoked response in man. Electroencephalogr Clin Neurophysiol 28:153–161
Gallinat J, Bottlender R, Juckel G, Munke-Puchner A, Stotz G, Kuss HJ, Mavrogiorgou P, Hegerl U (2000) The loudness dependency of the auditory evoked N1/P2-component as a predictor of the acute SSRI response in depression. Psychopharmacology 148:404–411
Hari R, Kaila K, Katila T, Tuomisto T, Varpula T (1982) Interstimulus interval dependence of the auditory vertex response and its magnetic counterpart: implications for their neural generation. Electroencephalogr Clin Neurophysiol 54:561–569
Hershman KM, Freedman R, Bickford PC (1995) GABAB antagonists diminish the inhibitory gating of auditory response in the rat hippocampus. Neurosci Lett 190:133–136
Höffken O, Grehl T, Dinse HR, Tegenthoff M, Bach M (2008) Paired-pulse behavior of visually evoked potentials recorded in human visual cortex using patterned paired-pulse stimulation. Exp Brain Res 188:427–435
Hussman JP (2001) Suppressed GABAergic inhibition as a common factor in suspected etiologies of autism. J Autism Dev Disord 31(2):247–248
Inui K, Urakawa T, Yamashiro K, Otsuru N, Nishihara M, Takeshima Y, Kakigi R (2010a) Non-linear laws of echoic memory and auditory change detection in humans. BMC Neurosci 11:80
Inui K, Urakawa T, Yamashiro K, Otsuru N, Takeshima Y, Nishihara M, Kakigi R (2010b) Echoic memory of a single pure tone indexed by change-related brain activity. BMC Neurosci 11:135
Inui K, Tsuruhara A, Nakagawa K, Nishihara M, Kodaira M, Motomura E, Kakigi R (2013) Prepulse inhibition of change-related P50m no correlation with P50m gating. Springerplus 2:588
Inui K, Nakagawa K, Nishihara M, Motomura E, Kakigi R (2016) Inhibition in the human auditory cortex. PLoS ONE 11:e0155972
Inui K, Takeuchi N, Sugiyama S, Motomura E, Nishihara M (2018) GABAergic mechanisms involved in the prepulse inhibition of auditory evoked cortical responses in humans. PLoS ONE 13:e0190481
Jensen KS, Oranje B, Wienberg M, Glenthøj BY (2008) The effects of increased serotonergic activity on human sensory gating and its neural generators. Psychopharmacology 196:631–641
Kirischuk S, Clements JD, Grantyn R (2002) Presynaptic and postsynaptic mechanisms underlie paired pulse depression at single GABAergic boutons in rat collicular cultures. J Physiol 15(543):99–116
Lijffijt M, Moeller FG, Boutros NN, Burroughs S, Lane SD, Steinberg JL, Swann AC (2009) The role of age, gender, education, and intelligence in P50, N100, and P200 auditory sensory gating. J Psychophysiol 23:52–62
Ma J, Leung LS (2011) GABA(B) receptor blockade in the hippocampus affects sensory and sensorimotor gating in Long-Evans rats. Psychopharmacology 217:167–176
McLaughlin DF, Kelly EF (1993) Evoked potentials as indices of adaptation in the somatosensory system in humans: a review and prospectus. Brain Res Brain Res Rev 18:151–206
Muller CL, Anacker A, Veenstra-VanderWeele J (2016) The serotonin system in autism spectrum disorder: from biomarker to animal models. Neuroscience 321:24–41
Nakagawa K, Inui K, Yuge L, Kakigi R (2014) Inhibition of somatosensory-evoked cortical responses by a weak leading stimulus. Neuroimage 101:416–424
Nishihara M, Inui K, Motomura E, Otsuru N, Ushida T, Kakigi R (2011) Auditory N1 as a change-related automatic response. Neurosci Res 71:145–148
Nishihara M, Inui K, Morita T, Kodaira M, Mochizuki H, Otsuru N, Kakigi R (2014) Echoic memory: investigation of its temporal resolution by auditory offset cortical responses. PLoS ONE 9:e106553
Ohoyama K, Motomura E, Inui K, Nishihara M, Otsuru N, Oi M, Kakigi R, Okada M (2012) Memory-based pre-attentive auditory N1 elicited by sound movement. Neurosci Res 73:248–251
Otsuru N, Tsuruhara A, Motomura E, Tanii H, Nishihara M, Inui K, Kakigi R (2012) Effects of acute nicotine on auditory change-related cortical responses. Psychopharmacology 224:327–335
Patterson JV, Hetrick WP, Boutros NN, Jin Y, Sandman C, Stern H, Potkin S, Bunney WE Jr (2008) P50 sensory gating ratios in schizophrenics and controls: a review and data analysis. Psychiatry Res 158:226–247
Pérez-González D, Malmierca MS (2014) Adaptation in the auditory system: an overview. Front Integr Neurosci 8:19
Pouretemad HR, Thompson PJ, Fenwick PB (1998) Impaired sensorimotor gating in patients with non-epileptic seizures. Epilepsy Res 31:1–12
Ritter W, Vaughan HG Jr, Costa LD (1968) Orienting and habituation to auditory stimuli: a study of short term changes in average evoked responses. Electroencephalogr Clin Neurophysiol 25:550–556
Rosburg T, Mager R (2021) The reduced auditory evoked potential component N1 after repeated stimulation: refractoriness hypothesis vs. habituation account. Hear Res 400:108140
Rosburg T, Trautner P, Korzyukov OA, Boutros NN, Schaller C, Elger CE, Kurthen M (2004) Short-term habituation of the intracranially recorded auditory evoked potentials P50 and N100. Neurosci Lett 372:245–249
Rosburg T, Trautner P, Elger CE, Kurthen M (2009) Attention effects on sensory gating–intracranial and scalp recordings. Neuroimage 48:554–563
Siegel C, Waldo M, Mizner G, Adler LE, Freedman R (1984) Deficits in sensory gating in schizophrenic patients and their relatives. Evidence obtained with auditory evoked responses. Arch Gen Psychiatry 41:607–612
Swerdlow NR, Shoemaker JM, Stephany N, Wasserman L, Ro HJ, Geyer MA (2002) Prestimulus effects on startle magnitude: sensory or motor? Behav Neurosci 116:672–681
Takeuchi N, Sugiyama S, Inui K, Kanemoto K, Nishihara M (2017) New paradigm for auditory paired pulse suppression. PLoS ONE 12:e0177747
Takeuchi N, Kinukawa T, Sugiyama S, Inui K, Nishihara M (2020) Test-retest reliability of prepulse inhibition paradigm using auditory evoked potentials. Neurosci Res 170:187–194
Takeuchi N, Fujita K, Kinukawa T, Sugiyama S, Kanemoto K, Nishihara M, Inui K (2021) Test–retest reliability of paired pulse suppression paradigm using auditory change-related response. J of neurosci med 352:109–087
Urakawa T, Inui K, Yamashiro K, Tanaka E, Kakigi R (2010) Cortical dynamics of visual change detection based on sensory memory. Neuroimage 52:302–308
Waldbaum S, Dudek FE (2009) Single and repetitive paired-pulse suppression: a parametric analysis and assessment of usefulness in epilepsy research. Epilepsia 50:904–916
Wassef A, Baker J, Kochan LD (2003) GABA and schizophrenia: a review of basic science and clinical studies. J Clin Psychopharmacol 23(6):601–640
Yamashiro K, Inui K, Otsuru N, Kakigi R (2011) Change-related responses in the human auditory cortex: an MEG study. Psychophysiology 48:23–30
Funding
The funding was supported by Japan Society for the Promotion of Science [Grant Nos. JP18K07619, JP16K10262].
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Claude Alain.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Takeuchi, N., Fujita, K., Taniguchi, T. et al. Mechanisms of Long-Latency Paired Pulse Suppression: MEG Study. Brain Topogr 35, 241–250 (2022). https://doi.org/10.1007/s10548-021-00878-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10548-021-00878-6