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Dopamine and beta-band oscillations differentially link to striatal value and motor control.

ABSTRACT: Parkinson's disease is characterized by decreased dopamine and increased beta-band oscillatory activity accompanying debilitating motor and mood impairments. Coordinate dopamine-beta opposition is considered a normative rule for basal ganglia function. We report a breakdown of this rule. We developed multimodal systems allowing the first simultaneous, chronic recordings of dopamine release and beta-band activity in the striatum of nonhuman primates during behavioral performance. Dopamine and beta signals were anticorrelated over seconds-long time frames, in agreement with the posited rule, but at finer time scales, we identified conditions in which these signals were modulated with the same polarity. These measurements demonstrated that task-elicited beta suppressions preceded dopamine peaks and that relative dopamine-beta timing and polarity depended on reward value, performance history, movement, and striatal domain. These findings establish a new view of coordinate dopamine and beta signaling operations, critical to guide novel strategies for diagnosing and treating Parkinson's disease and related neurodegenerative disorders.

SUBMITTER: Schwerdt HN

PROVIDER: S-EPMC7518859 | biostudies-literature | 2020 Sep

REPOSITORIES: biostudies-literature

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Dopamine and beta-band oscillations differentially link to striatal value and motor control.

Schwerdt H N HN Amemori K K Gibson D J DJ Stanwicks L L LL Yoshida T T Bichot N P NP Amemori S S Desimone R R Langer R R Cima M J MJ Graybiel A M AM

Science advances 20200925 39

Parkinson's disease is characterized by decreased dopamine and increased beta-band oscillatory activity accompanying debilitating motor and mood impairments. Coordinate dopamine-beta opposition is considered a normative rule for basal ganglia function. We report a breakdown of this rule. We developed multimodal systems allowing the first simultaneous, chronic recordings of dopamine release and beta-band activity in the striatum of nonhuman primates during behavioral performance. Dopamine and bet ...[more]

PMID: 32978148

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Project description:Striatal oscillatory activity is associated with movement, reward, and decision-making, and observed in several interacting frequency bands. Local field potential recordings in rodent striatum show dopamine- and reward-dependent transitions between two states: a "spontaneous" state involving ? (?15-30 Hz) and low ? (?40-60 Hz), and a state involving ? (?4-8 Hz) and high ? (?60-100 Hz) in response to dopaminergic agonism and reward. The mechanisms underlying these rhythmic dynamics, their interactions, and their functional consequences are not well understood. In this paper, we propose a biophysical model of striatal microcircuits that comprehensively describes the generation and interaction of these rhythms, as well as their modulation by dopamine. Building on previous modeling and experimental work suggesting that striatal projection neurons (SPNs) are capable of generating ? oscillations, we show that networks of striatal fast-spiking interneurons (FSIs) are capable of generating ?/? (ie, 2 to 6 Hz) and ? rhythms. Under simulated low dopaminergic tone our model FSI network produces low ? band oscillations, while under high dopaminergic tone the FSI network produces high ? band activity nested within a ?/? oscillation. SPN networks produce ? rhythms in both conditions, but under high dopaminergic tone, this ? oscillation is interrupted by ?/?-periodic bursts of ?-frequency FSI inhibition. Thus, in the high dopamine state, packets of FSI ? and SPN ? alternate at a ?/? timescale. In addition to a mechanistic explanation for previously observed rhythmic interactions and transitions, our model suggests a hypothesis as to how the relationship between dopamine and rhythmicity impacts motor function. We hypothesize that high dopamine-induced periodic FSI ?-rhythmic inhibition enables switching between ?-rhythmic SPN cell assemblies representing the currently active motor program, and thus that dopamine facilitates movement in part by allowing for rapid, periodic shifts in motor program execution.

Dataset Information

Dopamine and beta-band oscillations differentially link to striatal value and motor control.

Publications

Dopamine and beta-band oscillations differentially link to striatal value and motor control.

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