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Special Communication |

Neural Oscillations and Synchrony in Brain Dysfunction and Neuropsychiatric Disorders It’s About Time

Daniel H. Mathalon, PhD, MD1,2,3; Vikaas S. Sohal, MD, PhD1,4
[+] Author Affiliations
1Department of Psychiatry, University of California, San Francisco
2Department of Biomedical Sciences, University of California, San Francisco
3Mental Health Service, San Francisco Veterans Affairs Health Care System, San Francisco, California
4Department of Neuroscience, University of California, San Francisco
JAMA Psychiatry. 2015;72(8):840-844. doi:10.1001/jamapsychiatry.2015.0483.
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Neural oscillations are rhythmic fluctuations over time in the activity or excitability of single neurons, local neuronal populations or “assemblies,” and/or multiple regionally distributed neuronal assemblies. Synchronized oscillations among large numbers of neurons are evident in electrocorticographic, electroencephalographic, magnetoencephalographic, and local field potential recordings and are generally understood to depend on inhibition that paces assemblies of excitatory neurons to produce alternating temporal windows of reduced and increased excitability. Synchronization of neural oscillations is supported by the extensive networks of local and long-range feedforward and feedback bidirectional connections between neurons. Here, we review some of the major methods and measures used to characterize neural oscillations, with a focus on gamma oscillations. Distinctions are drawn between stimulus-independent oscillations recorded during resting states or intervals between task events, stimulus-induced oscillations that are time locked but not phase locked to stimuli, and stimulus-evoked oscillations that are both time and phase locked to stimuli. Synchrony of oscillations between recording sites, and between the amplitudes and phases of oscillations of different frequencies (cross-frequency coupling), is described and illustrated. Molecular mechanisms underlying gamma oscillations are also reviewed. Ultimately, understanding the temporal organization of neuronal network activity, including interactions between neural oscillations, is critical for elucidating brain dysfunction in neuropsychiatric disorders.

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Figure 1.
Evoked and Induced Gamma Oscillations

A, Evoked oscillations result when a stimulus resets the phase of ongoing oscillations or evokes new oscillations such that their phases are consistently aligned across trials. ERP indicates event-related potential. Evoked oscillations survive averaging across trials and are present in the ERP. They are reflected in evoked power and intertrial coherence. In this example, evoked oscillations are not reflected in total power estimates because their amplitudes did not increase relative to the prestimulus baseline. B, Induced oscillations result when a stimulus induces an increase in the amplitude of oscillations without resetting their phases across trials. Random phase of induced oscillations results in (1) no surviving oscillations when trials are averaged to generate the ERP; (2) no evoked power (calculated from the ERP); and (3) no intertrial coherence. In parts A and B, the power spectrum can be calculated for the prestimulus baseline electroencephalographic (EEG) intervals followed by averaging (single trial), or it can be calculated from the ERP baseline. The gamma oscillatory power evident in the single trials is lost during averaging over trials and is not present in the power spectrum of the ERP baseline. Because prestimulus baseline EEG oscillations are not time locked to events, their power is quantified as a power spectrum calculated over the entire time epoch (left panels).

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Figure 2.
Cross-Site Gamma Phase Coherence

On the left side, 2 hypothetical cortical sources of gamma oscillations, a frontal source (site I [red]) and a parietal source (site II [blue]). In the middle, an overlay of oscillations from sites I and II for each single-trial electroencephalographic (EEG) epoch. The middle left shows relatively short phase lag (65°) between oscillations from sites I and II. The middle right shows relatively long phase lag (209°) between oscillations from sites I and II. On the right side, cross-site phase coherence reflects consistency of phase lag between sites I and II across trials. Gamma-phase coherence across sites is equivalent regardless of whether the phase lag between the gamma oscillations from the 2 sites is short or long. Furthermore, despite high phase coherence between sites over trials, the phases of the oscillations across trials at each site are not consistent (ie, low intertrial coherence).

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Figure 3.
Theta Phase–Gamma Power Cross-Frequency Coupling

Left, theta phase–gamma power cross-frequency coupling in EEG from a single recording site. Right, theta-gamma cross-frequency coupling between recording sites. site I (red) shows theta oscillation; site II (blue) shows gamma oscillation. Gamma oscillation magnitude increases during the peak of the theta oscillation, a common form of cross-frequency coupling.

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Figure 4.
Parvalbumin (PV) Interneuron–Pyramidal Neuron Microcircuit Underlying Neuronal Gamma Oscillation

Active pyramidal neurons excite PV interneurons, causing PV interneurons to spike and leading to inhibitory synaptic potentials in pyramidal neurons, silencing them. When this inhibition wears off, pyramidal neurons spike again, leading to reexcitation of the PV interneurons and starting a new cycle.

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