Trends in Neurosciences
OpinionNew insights into the relationship between dopamine, beta oscillations and motor function
Introduction
Brain activity is dominated by synchronised oscillations between populations of neurons. These oscillations appear as rhythmical fluctuations in both electroencephalographic (EEG) and local field potential (LFP) recordings (see Glossary), as well as in synchronised activity between cells. Whether these patterns have functional significance or are epiphenomenal is a major unresolved question in neuroscience. Oscillations in neuronal populations are generally characterised by the frequency at which they occur, and the past decade has seen growing interest in those oscillations occurring in the beta band (i.e. between 13 and 30 Hz). These are prominent in the human motor system, being recorded in the somatomotor cortex, the cerebellar system and basal ganglia (BG), where they behave in a task-dependent manner [1].
Nevertheless, the function of beta activity in the motor system remains unclear. Here, we will consider the possible role for beta activity in the BG–cortical motor loop, where interest has been heightened by the recent observation that beta activity is exaggerated in the BG of patients with Parkinson's disease (PD) and may contribute to their motor impairment (reviewed in 1, 2, 3, 4). Initially, beta oscillations were thought to be a marker of idling activity [5], but this theory has been superseded by the view that beta activity in the BG–cortical loop promotes tonic activity at the expense of voluntary movement 1, 6. This more recent hypothesis certainly captures some features of beta activity, such as its increase during tonic contractions and its suppression during voluntary movement [2]. However, this hypothesis has also been challenged 7, 8, 9, and it is essentially phenomenal, with limited heuristic value. Here, we will critically evaluate the evidence for and against this hypothesis, before refining and developing it into a more detailed model, which places beta activity in the context of emerging ideas about dopamine function. Clear experimental predictions to test such a model are outlined.
Section snippets
Current status: do beta oscillations promote tonic activity?
Support for the hypothesis that beta activity promotes tonic activity at the expense of voluntary movement comes from investigations of oscillatory activity at the cortical level 10, 11, 12 and relies on the fact that the BG and cortex are connected in a functional loop. As such, cortical beta levels are likely to be functionally related to beta levels in the BG, as revealed by magnetoencephalography (MEG) recordings in PD patients that show coherent beta activity in the two structures (Figure 1
An extended hypothesis of the function of BG–cortical beta
Although the quantitative importance of exaggerated beta synchrony in PD is still to be established, there remains some support for the general notion that BG–cortical beta activity biases against voluntary movement. This characterisation, however, fails to place beta activity in the context of other theories of BG function, and hence, its essentially phenomenal nature has limited heuristic value.
We propose that beta activity in the BG–cortical system provides an internal index of the
What is needed by way of experimental support?
We have refined and expanded upon the hypothesis that considers beta activity antikinetic. The arguments outlined above serve to explain several observations, particularly how pharmacological treatments can improve motor dysfunction in PD. The stage is now set for a direct demonstration that beta activity is dynamically suppressed by elevations in net dopamine, together with an explicit demonstration that motor-salient cues, whether external or internal, modulate tonic dopamine levels in the
Acknowledgements
We thank Bruno Averbeck and Mark Walton for comments on this article. This work was supported by the Medical Research Council, Cure Parkinson's Trust, Rosetrees Trust and National Institute for Health Research Oxford Biomedical Centre.
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