Human Oscillatory Brain Activity Near 40 Hz Coexists with Cognitive Temporal Binding

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1994 Nov 22

PMID 7972135

Citations 94

Authors

M Joliot

U Ribary

R Llinas

Affiliations

Soon will be listed here.

Abstract

Spontaneous oscillatory electrical activity at a frequency near 40 Hz in the human brain and its reset by sensory stimulation have been proposed to be related to cognitive processing and to the temporal binding of sensory stimuli. These experiments were designed to test this hypothesis and to determine specifically whether the minimal interval required to identify separate auditory stimuli correlates with the reset of the 40-Hz magnetic signal. Auditory clicks were presented at varying times, while magnetic activity was recorded from awake human subjects. Experimental and modeling results indicate a stimulus-interval-dependent response with a critical interval of 12-15 ms. At shorter intervals only one 40-Hz response, to the first stimulus, was observed. With longer intervals, a second 40-Hz wave abruptly appeared, which coincided with the subject's perception of a second distinct auditory stimulus. These results indicate that oscillatory activity near 40 Hz represents a neurophysiological correlate to the temporal processing of auditory stimuli. It also supports the view that 40-Hz activity not only relates to primary sensory processing, but also could reflect the temporal binding underlying cognition.

Citing Articles

Differential analgesic effects of high-frequency or accelerated intermittent theta burst stimulation of M1 on experimental tonic pain: Correlations with cortical activity changes assessed by TMS-EEG.

Tan B, Chen J, Liu Y, Lin Q, Wang Y, Shi S Neurotherapeutics. 2024; 21(6):e00451.

PMID: 39304439 PMC: 11585887. DOI: 10.1016/j.neurot.2024.e00451.

Network resonance and the auditory steady state response.

Johnson T, Gallagher A, Coulson S, Rangel L Sci Rep. 2024; 14(1):16799.

PMID: 39039107 PMC: 11263589. DOI: 10.1038/s41598-024-66697-4.

Altered dynamical integration/segregation balance during anesthesia-induced loss of consciousness.

Lord L, Carletti T, Fernandes H, Turkheimer F, Expert P Front Netw Physiol. 2023; 3:1279646.

PMID: 38116461 PMC: 10728865. DOI: 10.3389/fnetp.2023.1279646.

Does Electrophysiological Maturation Shape Language Acquisition?.

Menn K, Mannel C, Meyer L Perspect Psychol Sci. 2023; 18(6):1271-1281.

PMID: 36753616 PMC: 10623610. DOI: 10.1177/17456916231151584.

EEG and ECG Power Spectrum Analysis of Sedative Effects on Propofol-Anesthetized Rats with Electroacupuncture.

Zhu S, Ma J, Wang Z, Chai Q, Yan L, Song J Evid Based Complement Alternat Med. 2022; 2022:2440609.

PMID: 35668776 PMC: 9167085. DOI: 10.1155/2022/2440609.

References

Steriade M, Dossi R, Pare D, Oakson G . Fast oscillations (20-40 Hz) in thalamocortical systems and their potentiation by mesopontine cholinergic nuclei in the cat. Proc Natl Acad Sci U S A. 1991; 88(10):4396-400. PMC: 51666. DOI: 10.1073/pnas.88.10.4396. View

Madler C, Keller I, Schwender D, Poppel E . Sensory information processing during general anaesthesia: effect of isoflurane on auditory evoked neuronal oscillations. Br J Anaesth. 1991; 66(1):81-7. DOI: 10.1093/bja/66.1.81. View

Ribary U, Ioannides A, Singh K, Hasson R, Bolton J, Lado F . Magnetic field tomography of coherent thalamocortical 40-Hz oscillations in humans. Proc Natl Acad Sci U S A. 1991; 88(24):11037-41. PMC: 53068. DOI: 10.1073/pnas.88.24.11037. View

Crick F, Koch C . Some reflections on visual awareness. Cold Spring Harb Symp Quant Biol. 1990; 55:953-62. DOI: 10.1101/sqb.1990.055.01.089. View

Murthy V, Fetz E . Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. Proc Natl Acad Sci U S A. 1992; 89(12):5670-4. PMC: 49354. DOI: 10.1073/pnas.89.12.5670. View

Llinas R, Ribary U . Coherent 40-Hz oscillation characterizes dream state in humans. Proc Natl Acad Sci U S A. 1993; 90(5):2078-81. PMC: 46024. DOI: 10.1073/pnas.90.5.2078. View

Tiitinen H, Sinkkonen J, Reinikainen K, Alho K, Lavikainen J, Naatanen R . Selective attention enhances the auditory 40-Hz transient response in humans. Nature. 1993; 364(6432):59-60. DOI: 10.1038/364059a0. View

Moore B . Temporal analysis in normal and impaired hearing. Ann N Y Acad Sci. 1993; 682:119-36. DOI: 10.1111/j.1749-6632.1993.tb22964.x. View

Bressler S, Coppola R, Nakamura R . Episodic multiregional cortical coherence at multiple frequencies during visual task performance. Nature. 1993; 366(6451):153-6. DOI: 10.1038/366153a0. View

10.

Poppel E . Excitability cycles in central intermittency. Psychol Forsch. 1970; 34(1):1-9. DOI: 10.1007/BF00422860. View

11.

GALAMBOS R, Makeig S, Talmachoff P . A 40-Hz auditory potential recorded from the human scalp. Proc Natl Acad Sci U S A. 1981; 78(4):2643-7. PMC: 319406. DOI: 10.1073/pnas.78.4.2643. View

12.

KRISTOFFERSON A . Quantal and deterministic timing in human duration discrimination. Ann N Y Acad Sci. 1984; 423:3-15. DOI: 10.1111/j.1749-6632.1984.tb23413.x. View

13.

Basar E, Rosen B, Basar-Eroglu C, Greitschus F . The associations between 40 Hz-EEG and the middle latency response of the auditory evoked potential. Int J Neurosci. 1987; 33(1-2):103-17. DOI: 10.3109/00207458708985933. View

14.

Eckhorn R, Bauer R, Jordan W, Brosch M, Kruse W, Munk M . Coherent oscillations: a mechanism of feature linking in the visual cortex? Multiple electrode and correlation analyses in the cat. Biol Cybern. 1988; 60(2):121-30. DOI: 10.1007/BF00202899. View

15.

Gray C, Singer W . Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc Natl Acad Sci U S A. 1989; 86(5):1698-702. PMC: 286768. DOI: 10.1073/pnas.86.5.1698. View

16.

Ahissar E, Vaadia E . Oscillatory activity of single units in a somatosensory cortex of an awake monkey and their possible role in texture analysis. Proc Natl Acad Sci U S A. 1990; 87(22):8935-9. PMC: 55075. DOI: 10.1073/pnas.87.22.8935. View

17.

Llinas R, Grace A, Yarom Y . In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10- to 50-Hz frequency range. Proc Natl Acad Sci U S A. 1991; 88(3):897-901. PMC: 50921. DOI: 10.1073/pnas.88.3.897. View

18.

Pantev C, Makeig S, Hoke M, GALAMBOS R, Hampson S, Gallen C . Human auditory evoked gamma-band magnetic fields. Proc Natl Acad Sci U S A. 1991; 88(20):8996-9000. PMC: 52638. DOI: 10.1073/pnas.88.20.8996. View