Dynamic Network Communication as a Unifying Neural Basis for Cognition, Development, Aging, and Disease

Voytek, Bradley; Knight, Robert T.

doi:10.1016/j.biopsych.2015.04.016

Cited by 556Neural dynamics and brain functionFunctional Brain Connectivity StudiesNonlinear Dynamics and Pattern Formation

Dynamic Network Communication as a Unifying Neural Basis for Cognition, Development, Aging, and Disease

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Voytek, Bradley, Knight, Robert T.·2015·Biological Psychiatry

DOI 10.1016/j.biopsych.2015.04.016PMC PMC4443259

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Abstract

Perception, cognition, and social interaction depend upon coordinated neural activity. This coordination operates within noisy, overlapping, and distributed neural networks operating at multiple timescales. These networks are built upon a structural scaffolding with intrinsic neuroplasticity that changes with development, aging, disease, and personal experience. In this article, we begin from the perspective that successful interregional communication relies upon the transient synchronization between distinct low-frequency (<80 Hz) oscillations, allowing for brief windows of communication via phase-coordinated local neuronal spiking. From this, we construct a theoretical framework for dynamic network communication, arguing that these networks reflect a balance between oscillatory coupling and local population spiking activity and that these two levels of activity interact. We theorize that when oscillatory coupling is too strong, spike timing within the local neuronal population becomes too synchronous; when oscillatory coupling is too weak, spike timing is too disorganized. Each results in specific disruptions to neural communication. These alterations in communication dynamics may underlie cognitive changes associated with healthy development and aging, in addition to neurological and psychiatric disorders. A number of neurological and psychiatric disorders-including Parkinson's disease, autism, depression, schizophrenia, and anxiety-are associated with abnormalities in oscillatory activity. Although aging, psychiatric and neurological disease, and experience differ in the biological changes to structural gray or white matter, neurotransmission, and gene expression, our framework suggests that any resultant cognitive and behavioral changes in normal or disordered states or their treatment are a product of how these physical processes affect dynamic network communication.

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Spontaneous background neural 'noise' is necessary to prevent excessive local overcoupling.
“It has been hypothesized, for example, that spontaneous background neural “noise” is necessary to prevent excessive local overcoupling [31].”
From EEG power at 3 months in infants at high familial risk for autism (2017) · cites this paper as [31]
Decreased power in higher frequencies can be seen when muscle activity is decreased, but also when spontaneous background neuronal firing activity is decreased.
“This decreased power in higher frequencies can be seen when muscle activity is decreased (as above), but also when spontaneous background neuronal firing activity is decreased [30, 31].”
From EEG power at 3 months in infants at high familial risk for autism (2017) · cites this paper as [31]

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[47]Szczepanski SM Crone NE Kuperman RA Auguste KI Parvizi J Knight RT Posner M Dynamic Changes in Phase-Amplitude Coupling Facilitate Spatial Attention Control in Fronto-Parietal Cortex Plos Biol 2014 12 e1001936 e1001914 PMC4144794 25157678
[102]The Organizaiton of Behavior The Organizaiton of Behavior 1949 New York John Wiley & Sons

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“Furthermore, disrupted network dynamics might be a result of more subtle changes (McCarthy et al., 2012; Kopell et al., 2014; Voytek and Knight, 2015), such as neurochemical shifts and changes in synaptic binding potentials and receptor density.”
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Authors: Voytek, B., & Knight, R. T.
Affiliations: University of California San Diego (US)
University of California, Berkeley (US)
Corresponding author: Voytek, Bradley
ORCID: Voytek, Bradley
Knight, Robert T.
Venue: Biological Psychiatry
Publisher: Elsevier BV
Published: 2015-06
Volume: 77
Issue: 12
Pages: 1089-1097
ISSN: 0006-3223 (ISSN-L)
DOI: 10.1016/j.biopsych.2015.04.016
PMC: PMC4443259
OpenAlex: W2142864695
Cited by: 556
References: 132
Citations by year: 2026: 72 · 2025: 70 · 2024: 64 · 2023: 60 · 2022: 48 · 2021: 50 · 2020: 44 · 2019: 46 · 2018: 28 · 2017: 35 · 2016: 27 · 2015: 11
FWCI: 3.31
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-nd
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
creativecommons.org/licenses/by-nc-nd/4.0/ (vor)
Locations: Biological Psychiatry (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (2r01ns021135-33)
National Institute of Neurological Disorders and Stroke (R37 NS21135-27, R37NS021135, R01 NS-021135)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
Physical Sciences › Computer Science › Computer Networks and Communications › Nonlinear Dynamics and Pattern Formation
Keywords: neural oscillations, low-frequency oscillations, oscillatory coupling, neuronal spiking, phase synchronization, neuroplasticity, cognitive development, brain aging, neurological disorders, mental illness, Parkinson's disease, autism spectrum disorder, depression, schizophrenia, anxiety, neural network theory
MeSH terms: Action Potentials, Aging, Animals, Brain, Brain Diseases, Cognition, Cortical Synchronization, Humans, Models, Neurological, Nerve Net, Neurons, Brain Waves

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Dynamic Network Communication as a Unifying Neural Basis for Cognition, Development, Aging, and Disease

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