Trends in Neurosciences
Volume 34, Issue 12, December 2011, Pages 611-618
Journal home page for Trends in Neurosciences

Opinion
New insights into the relationship between dopamine, beta oscillations and motor function

https://doi.org/10.1016/j.tins.2011.09.003Get rights and content

Synchronised neuronal oscillations at beta frequencies are prevalent in the human motor system, but their function is unclear. In this Opinion article, we propose that the levels of beta oscillations provide a measure of the likelihood that a new voluntary action will need to be actuated. Oscillatory beta activity is in turn modulated by net dopamine levels at sites of cortical input to the basal ganglia. We hypothesise that net dopamine levels are modulated in response to salient internal and external cues. Crucially, the resulting modulation of beta activity is predictive, enabling the appropriate prospective resourcing and preparation of potential actions. Loss of dopamine, as in Parkinson's disease, annuls this function, unless net dopaminergic activity can be elevated through medication.

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 Initially, beta oscillations were thought to be a marker of idling activity [5], but this theory has been superseded by the view that beta activity in the BG–cortical loop promotes tonic activity at the expense of voluntary movement 1, 6.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.

References (86)

  • N. Ray

    Local field potential beta activity in the subthalamic nucleus of patients with Parkinson's disease is associated with improvements in bradykinesia after dopamine and deep brain stimulation

    Exp. Neurol.

    (2008)
  • A.A. Kühn

    Pathological synchronisation in the subthalamic nucleus of patients with Parkinson's disease relates to both bradykinesia and rigidity

    Exp. Neurol.

    (2009)
  • H. Bronte-Stewart

    The STN beta-band profile in Parkinson's disease is stationary and shows prolonged attenuation after deep brain stimulation

    Exp. Neurol.

    (2009)
  • C. Chen

    Excessive synchronization of basal ganglia neurons at 20 Hz slows movement in Parkinson's disease

    Exp. Neurol.

    (2007)
  • C.C. Chen

    Stimulation of the subthalamic region at 20 Hz slows the development of grip force in Parkinson's disease

    Exp. Neurol.

    (2011)
  • A. Eusebio

    Effects of low-frequency stimulation of the subthalamic nucleus on movement in Parkinson's disease

    Exp. Neurol.

    (2008)
  • N. Fogelson

    Frequency dependent effects of subthalamic nucleus stimulation in Parkinson's disease

    Neurosci. Lett.

    (2005)
  • H.W. Berendse et al.

    Stage-dependent patterns of disturbed neural synchrony in Parkinson's disease

    Parkinsonism Relat. Disord.

    (2007)
  • L.M.F. Doyle

    Lateralization of event-related beta desynchronization in the EEG during pre-cued reaction time tasks

    Clin. Neurophysiol.

    (2005)
  • T.H. Donner

    Buildup of choice-predictive activity in human motor cortex during perceptual decision making

    Curr. Biol.

    (2009)
  • C. Loukas et al.

    Online prediction of self-paced hand-movements from subthalamic activity using neural networks in Parkinson's disease

    J. Neurosci. Methods

    (2004)
  • A.A. Kühn

    Increased beta activity in dystonia patients after drug-induced dopamine deficiency

    Exp. Neurol.

    (2008)
  • F.G. Gonon

    Nonlinear relationship between impulse flow and dopamine released by rat midbrain dopaminergic neurons as studied by in vivo electrochemistry

    Neuroscience

    (1988)
  • B.I. Hyland

    Firing modes of midbrain dopamine cells in the freely moving rat

    Neuroscience

    (2002)
  • W. Schultz

    Behavioral dopamine signals

    Trends Neurosci.

    (2007)
  • W. Schultz

    Getting formal with dopamine and reward

    Neuron

    (2002)
  • J.C. Horvitz

    Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events

    Neuroscience

    (2000)
  • K. Chergui

    Nonlinear relationship between impulse flow, dopamine release and dopamine elimination in the rat brain in vivo

    Neuroscience

    (1994)
  • C. Dugast

    Continuous in vivo monitoring of evoked dopamine release in the rat nucleus accumbens by amperometry

    Neuroscience

    (1994)
  • M.E. Rice et al.

    Dopamine spillover after quantal release: rethinking dopamine transmission in the nigrostriatal pathway

    Brain Res. Rev.

    (2008)
  • A.J. Jurkowski

    Variable foreperiod deficits in Parkinson's disease: dissociation across reflexive and voluntary behaviors

    Brain Cogn.

    (2005)
  • D. Devos

    Predominance of the contralateral movement-related activity in the subthalamo-cortical loop

    Clin. Neurophysiol.

    (2006)
  • P.J. Magill

    Dopamine regulates the impact of the cerebral cortex on the subthalamic nucleus-globus pallidus network

    Neuroscience

    (2001)
  • P. Brown et al.

    Basal ganglia local field potential activity: character and functional significance in the human

    Clin. Neurophysiol.

    (2005)
  • M. Kringelbach

    Translational principles of deep brain stimulation

    Nat. Rev. Neurosci.

    (2007)
  • A. Leblois

    Competition between feedback loops underlies normal and pathological dynamics in the basal ganglia

    J. Neurosci.

    (2006)
  • A. Leblois

    Late emergence of synchronized oscillatory activity in the pallidum during progressive parkinsonism

    Eur. J. Neurosci.

    (2007)
  • T. Gilbertson

    Existing motor state is favored at the expense of new movement during 13-35 Hz oscillatory synchrony in the human corticospinal system

    J. Neurosci.

    (2005)
  • B. Pastotter

    Inhibition of return arises from inhibition of response processes: an analysis of oscillatory beta activity

    J. Cogn. Neurosci.

    (2008)
  • B.C.M. van Wijk

    A role of beta oscillatory synchrony in biasing response competition?

    Cereb. Cortex

    (2009)
  • E. Lalo

    Patterns of bidirectional communication between cortex and basal ganglia during movement in patients with Parkinson disease

    J. Neurosci.

    (2008)
  • V. Litvak

    Resting oscillatory cortico-subthalamic connectivity in patients with Parkinson's disease

    Brain

    (2011)
  • A.G. Androulidakis

    Corrective movements in response to displacements in visual feedback are more effective during periods of 13-35 Hz oscillatory synchrony in the human corticospinal system

    Eur. J. Neurosci.

    (2006)
  • Cited by (0)

    View full text