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Normal and pathological oscillatory communication in the brain

Key Points

  • The remarkable processing capabilities of the brain rely on efficient communication between the huge number of neurons and neuronal assemblies that constitute functionally specialized units. Abundant anatomical connections form the structural basis of communication. Functionally, the synchronization of oscillatory neuronal activity has increasingly been recognized as a mechanism for long-range communication.

  • Studies of the insect olfactory system provide the most direct evidence that oscillatory communication is behaviourally relevant. These and other studies point towards several mechanisms that funtion on different spatial scales to support interneuronal communication. Filtering and resonance phenomena indicate the dependence of neuronal activity on the frequency content of the input. Specific structural connectivity underlies the emergence of particular network properties that facilitate specific computations by spatiotemporal patterns of excitation and inhibition.

  • New analytical methods have allowed the non-invasive investigation of frequency-specific long-range communication in the human brain with magnetoencephalographic (MEG) recordings.

  • Recent studies in humans and monkeys have provided new evidence for the physiological relevance of oscillatory synchronization in motor and cognitive functions. Synchronization in the beta frequency band seems to have a particularly important role in long-range communication. The functional relevance of desynchronization processes is also being increasingly recognized, and specific spatiotemporal patterns of synchronization desynchronization have been directly related to attentional processes and behavioural performance.

  • In the human motor system, oscillations in the primary motor cortex modulate the firing rate of spinal motor neurons. This modulation is evident as oscillatory coupling between motor cortex activity and muscle activity.

  • Electrophysiological recordings of basal ganglia-thalamocortical circuits in healthy monkeys, a monkey model of Parkinson's disease and patients with Parkinson's disease have provided new insights into the functional roles of oscillations and oscillatory synchronization in normal and disturbed motor behaviour. Specifically, enhanced beta and reduced gamma oscillations are associated with the poverty and slowness of movement that is characteristic of Parkinson's disease. In addition, tremor seems to arise from abnormal synchronization of oscillations in several cortical and subcortical brain areas.

  • Chronic high-frequency deep brain stimulation, which can be delivered through electrodes that have been implanted in specific basal ganglia target structures, greatly improves motor symptoms in patients with Parkinson's disease, probably through desynchronizing effects.

  • Pathological changes in long-range synchronization are also evident in other movement disorders, as well as in neuropsychiatric diseases. Further work is needed to better understand the mechanisms that govern oscillatory communication and the consequences of disturbed communication. Hopefully, these studies will lead to the development of new therapeutic approaches.

Abstract

The huge number of neurons in the human brain are connected to form functionally specialized assemblies. The brain's amazing processing capabilities rest on local communication within and long-range communication between these assemblies. Even simple sensory, motor and cognitive tasks depend on the precise coordination of many brain areas. Recent improvements in the methods of studying long-range communication have allowed us to address several important questions. What are the common mechanisms that govern local and long-range communication and how do they relate to the structure of the brain? How does oscillatory synchronization subserve neural communication? And what are the consequences of abnormal synchronization?

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Figure 1: Oscillatory communication in the insect olfactory system.
Figure 2: Long-range synchronization in a visual attention-related network detected with whole-head magnetoencephalography (MEG).
Figure 3: Long-range oscillatory network that underlies 6–9 Hz movement discontinuities.
Figure 4: Oscillatory interactions in the beta band in the monkey cortex during an isometric contraction task.
Figure 5: The basal ganglia circuit.
Figure 6: Long-range synchronization in Parkinson's disease.

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Acknowledgements

We thank G. Laurent and the members of our lab for helpful comments on the manuscript. We apologize to those whose work was not cited due to space limitation. We gratefully acknowledge support by the Volkswagen Foundation and the German Research Foundation.

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Correspondence to Alfons Schnitzler.

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Glossary

FREQUENCY BANDS

Neural oscillations have been classified into different frequency bands (delta, 1–3 Hz; theta, 4–7 Hz; alpha, 8–13 Hz; beta, 14–30 Hz; gamma, 30–80 Hz; fast, 80–200 Hz; ultra fast, 200–600 Hz).

LOCAL FIELD POTENTIAL

(LFP). LFPs represent extracellularly recorded voltage fluctuations of a local neuronal population.

EXCITATORY (INHIBITORY) POSTSYNAPTIC POTENTIAL

Membrane depolarisation (hyperpolarization) of the postsynaptic neuron following excitatory (inhibitory) input.

PHASE-LOCKED

Phase locked action potentials occur at specific times in the oscillatory cycle of a local field potential.

DYNAMIC IMAGING OF COHERENT SOURCES

(DICS). Analysis technique that can compute tomographic functional maps of oscillatory power and coherence.

ELECTROMYOGRAM

Recording of electrical muscle activity.

COHERENCE

A frequency-domain measure of neuronal interaction normalized between 0 and 1. High values indicate dependence of two oscillations.

AGONIST AND ANTAGONIST

The antagonist is a muscle that counteracts the effect of another muscle, the agonist.

ISOMETRIC CONTRACTION

Static muscle contraction that occurs without movement.

CORTICOMUSCULAR COHERENCE

Coherence between cortical activity and muscle activity.

DEEP BRAIN STIMULATION

Continuous therapeutic electric stimulation of subcortical areas at high frequencies (130 Hz) using chronically implanted electrodes.

AKINESIA

Poverty and slowness of movement.

MPTP MODEL

Animals treated with the neurotoxic substance MPTP (1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine) develop symptoms of Parkinson's disease.

TOURETTE SYNDROME

A childhood-onset disorder that is characterized by irregular motor tics and vocalizations. It is often accompanied by obsessive-compulsive behavioural disturbances.

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Schnitzler, A., Gross, J. Normal and pathological oscillatory communication in the brain. Nat Rev Neurosci 6, 285–296 (2005). https://doi.org/10.1038/nrn1650

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