Literature DB >> 27469163

Neural mechanisms of transient neocortical beta rhythms: Converging evidence from humans, computational modeling, monkeys, and mice.

Maxwell A Sherman1, Shane Lee2, Robert Law2, Saskia Haegens3, Catherine A Thorn2, Matti S Hämäläinen4, Christopher I Moore2, Stephanie R Jones5.   

Abstract

Human neocortical 15-29-Hz beta oscillations are strong predictors of perceptual and motor performance. However, the mechanistic origin of beta in vivo is unknown, hindering understanding of its functional role. Combining human magnetoencephalography (MEG), computational modeling, and laminar recordings in animals, we present a new theory that accounts for the origin of spontaneous neocortical beta. In our MEG data, spontaneous beta activity from somatosensory and frontal cortex emerged as noncontinuous beta events typically lasting <150 ms with a stereotypical waveform. Computational modeling uniquely designed to infer the electrical currents underlying these signals showed that beta events could emerge from the integration of nearly synchronous bursts of excitatory synaptic drive targeting proximal and distal dendrites of pyramidal neurons, where the defining feature of a beta event was a strong distal drive that lasted one beta period (∼50 ms). This beta mechanism rigorously accounted for the beta event profiles; several other mechanisms did not. The spatial location of synaptic drive in the model to supragranular and infragranular layers was critical to the emergence of beta events and led to the prediction that beta events should be associated with a specific laminar current profile. Laminar recordings in somatosensory neocortex from anesthetized mice and awake monkeys supported these predictions, suggesting this beta mechanism is conserved across species and recording modalities. These findings make several predictions about optimal states for perceptual and motor performance and guide causal interventions to modulate beta for optimal function.

Entities:  

Keywords:  Parkinson's disease; beta rhythm; computational modeling; magnetoencephalography; sensorimotor processing

Mesh:

Year:  2016        PMID: 27469163      PMCID: PMC4995995          DOI: 10.1073/pnas.1604135113

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  63 in total

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Authors:  K S Rockland; D N Pandya
Journal:  Brain Res       Date:  1979-12-21       Impact factor: 3.252

2.  Pharmacologically induced and stimulus evoked rhythmic neuronal oscillatory activity in the primary motor cortex in vitro.

Authors:  N Yamawaki; I M Stanford; S D Hall; G L Woodhall
Journal:  Neuroscience       Date:  2007-11-01       Impact factor: 3.590

3.  Neuronal synchronization along the dorsal visual pathway reflects the focus of spatial attention.

Authors:  Markus Siegel; Tobias H Donner; Robert Oostenveld; Pascal Fries; Andreas K Engel
Journal:  Neuron       Date:  2008-11-26       Impact factor: 17.173

4.  Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships.

Authors:  D Contreras; M Steriade
Journal:  J Neurosci       Date:  1995-01       Impact factor: 6.167

Review 5.  Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena.

Authors:  U Mitzdorf
Journal:  Physiol Rev       Date:  1985-01       Impact factor: 37.312

6.  Laminar organization of thalamic projections to the rat neocortex.

Authors:  M Herkenham
Journal:  Science       Date:  1980-02-01       Impact factor: 47.728

7.  On the human sensorimotor-cortex beta rhythm: sources and modeling.

Authors:  O Jensen; P Goel; N Kopell; M Pohja; R Hari; B Ermentrout
Journal:  Neuroimage       Date:  2005-04-07       Impact factor: 6.556

Review 8.  Thalamic mechanisms of EEG alpha rhythms and their pathological implications.

Authors:  Stuart W Hughes; Vincenzo Crunelli
Journal:  Neuroscientist       Date:  2005-08       Impact factor: 7.519

Review 9.  Functions of the frontal cortex of the rat: a comparative review.

Authors:  B Kolb
Journal:  Brain Res       Date:  1984-11       Impact factor: 3.252

10.  Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex.

Authors:  Timo van Kerkoerle; Matthew W Self; Bruno Dagnino; Marie-Alice Gariel-Mathis; Jasper Poort; Chris van der Togt; Pieter R Roelfsema
Journal:  Proc Natl Acad Sci U S A       Date:  2014-09-09       Impact factor: 11.205

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  109 in total

1.  Frequency Shifts and Depth Dependence of Premotor Beta Band Activity during Perceptual Decision-Making.

Authors:  Chandramouli Chandrasekaran; Iliana E Bray; Krishna V Shenoy
Journal:  J Neurosci       Date:  2019-01-03       Impact factor: 6.167

Review 2.  The effect of STN DBS on modulating brain oscillations: consequences for motor and cognitive behavior.

Authors:  Fabian J David; Miranda J Munoz; Daniel M Corcos
Journal:  Exp Brain Res       Date:  2020-06-03       Impact factor: 1.972

3.  Dual origins of measured phase-amplitude coupling reveal distinct neural mechanisms underlying episodic memory in the human cortex.

Authors:  Alex P Vaz; Robert B Yaffe; John H Wittig; Sara K Inati; Kareem A Zaghloul
Journal:  Neuroimage       Date:  2017-01-06       Impact factor: 6.556

Review 4.  When brain rhythms aren't 'rhythmic': implication for their mechanisms and meaning.

Authors:  Stephanie R Jones
Journal:  Curr Opin Neurobiol       Date:  2016-07-09       Impact factor: 6.627

5.  Waveform changes with the evolution of beta bursts in the human subthalamic nucleus.

Authors:  Chien-Hung Yeh; Bassam Al-Fatly; Andrea A Kühn; Anders C Meidahl; Gerd Tinkhauser; Huiling Tan; Peter Brown
Journal:  Clin Neurophysiol       Date:  2020-06-29       Impact factor: 3.708

6.  Cell-Type Specific Burst Firing Interacts with Theta and Beta Activity in Prefrontal Cortex During Attention States.

Authors:  B Voloh; T Womelsdorf
Journal:  Cereb Cortex       Date:  2018-12-01       Impact factor: 5.357

7.  Beta oscillations reflect supramodal information during perceptual judgment.

Authors:  Saskia Haegens; José Vergara; Román Rossi-Pool; Luis Lemus; Ranulfo Romo
Journal:  Proc Natl Acad Sci U S A       Date:  2017-12-11       Impact factor: 11.205

8.  Phase reorganization leads to transient β-LFP spatial wave patterns in motor cortex during steady-state movement preparation.

Authors:  Michael E Rule; Carlos Vargas-Irwin; John P Donoghue; Wilson Truccolo
Journal:  J Neurophysiol       Date:  2018-02-14       Impact factor: 2.714

9.  Beta Oscillations in Working Memory, Executive Control of Movement and Thought, and Sensorimotor Function.

Authors:  Robert Schmidt; Maria Herrojo Ruiz; Bjørg E Kilavik; Mikael Lundqvist; Philip A Starr; Adam R Aron
Journal:  J Neurosci       Date:  2019-10-16       Impact factor: 6.167

Review 10.  Working Memory 2.0.

Authors:  Earl K Miller; Mikael Lundqvist; André M Bastos
Journal:  Neuron       Date:  2018-10-24       Impact factor: 17.173

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