Encyclopedia of Computational Neuroscience

Living Edition
| Editors: Dieter Jaeger, Ranu Jung

Basal Ganglia: Beta Oscillations

  • Rafal BogaczEmail author
Living reference work entry
DOI: https://doi.org/10.1007/978-1-4614-7320-6_82-1

Keywords

Basal Ganglion Transcranial Magnetic Stimulation Local Field Potential Effective Connectivity Beta Power 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Definition

Beta oscillations are defined as the oscillations in neural activity with frequencies between 13 and 30 Hz (Fig. 1). In the basal ganglia, the power of beta oscillations is significantly increased in Parkinson’s disease (Hammond et al. 2007).
Fig. 1

One second of local field potentials recorded from internal segment of globus pallidus (top panel) and subthalamic nucleus (bottom panel) from a patient with Parkinson’s disease who was off medications (Reproduced from Brown et al. (2001) with permission)

Relationship to Behavior

The power of beta oscillations is reduced prior to and during movements in both the cortex and basal ganglia (see Engel and Fries 2010 for review) and increased during tonic contractions (Baker et al. 1997). Consequently, it has been suggested that beta oscillations are related to maintaining the current body posture (Engel and Fries 2010). The causal influence of beta oscillations on inhibition of movement is suggested by observations that stimulation at beta frequency with transcranial magnetic stimulation (Pogosyan et al. 2009) and with deep-brain stimulation (Chen et al. 2007) results in slower movements.

Relationship with Symptoms

The relationship between beta oscillations and inhibition of movements discussed above suggests that the increased beta power in Parkinson’s disease may directly relate to the impaired movements observed in the disease (Brown 2007). This hypothesis is supported by the observation that the power of beta oscillations is reduced by the treatments that alleviate symptoms, namely, dopaminergic medications and high-frequency (>100 Hz) deep-brain stimulation of subthalamic nucleus (STN) (Hammond et al. 2007). Furthermore, the patients with the best improvement in motor skills due to medications also have the largest reduction in beta power in STN after taking the medications (Kuhn et al. 2006).

Models of the Effects of Beta Oscillations

Simulations demonstrated that the exaggerated oscillatory activity leads to movement difficulties possibly because the thalamic neurons (see Fig. 2) become entrained to the excessively oscillatory input from basal ganglia and are no longer able to transmit sensorimotor signals from the cortex (Rubin and Terman 2004). Additionally, an analysis of neural activity in the external segment of globus pallidus (GPe) using information theory showed reduced entropy during beta oscillations in rats, suggesting that the beta oscillations limit the amount of information transmitted by the neurons in the basal ganglia (Cruz et al. 2009).
Fig. 2

Subset of connectivity in the cortico-basal-ganglia-thalamic circuit. Black rectangles denote brain structures, and the rectangle labeled “Output” denotes the output nuclei of the basal ganglia comprised of the internal segment of globus pallidus and substantia nigra pars reticulata. Green arrows and red lines with circles denote excitatory and inhibitory connections, respectively. Blue dashed contours indicate sub-circuits that have been shown to generate beta oscillations in simulations

Origin of Beta Oscillations

Parkinson’s disease is caused by the death of dopaminergic neurons which project throughout the basal ganglia and modulate synaptic transmission and plasticity. However, the exaggerated beta oscillations do not appear immediately after the death of these neurons, but only several days later (Mallet et al. 2008a). This suggests that the beta oscillations result from the adaptations in the network following the reduced dopamine level.

It is still uncertain which of the changes in the connectivity and the levels of neuronal activity, occurring in Parkinson’s disease, trigger beta oscillations. Furthermore, due to the complex connectivity in the cortico-basal-ganglia-thalamic circuit (Fig. 2), it is still unclear in which part of the circuit the beta oscillations are generated. The circuit contains many feedback loops, and it is known that neuronal populations connected in loops can generate oscillations (Tiesinga and Sejnowski 2009).

One of the parts of the circuit which is thought to be critical for generation of Parkinsonian beta oscillations is a sub-circuit composed of STN and GPe (Bevan et al. 2002). Its role is suggested by observations that the beta oscillations are prominent in this network (Mallet et al. 2008b), this sub-circuit was shown to be able to produce slower (delta) oscillations in vitro (Plenz and Kital 1999), and blocking connections between STN and GPe abolishes excessive beta oscillations (Tachibana et al. 2011). Additionally, interactions between the STN-GPe network and cortex are likely to play important role in generating Parkinsonian beta, because the cortex and STN become coherent in the disease (Mallet et al. 2008b) and blocking connections between the cortex and STN abolishes excessive beta oscillations (Tachibana et al. 2011).

Computational Models of Beta Generation

Three sub-circuits containing feedback loops (indicated by blue contours in Fig. 2) have been shown to generate beta oscillation in simulations. First, models of the STN-GPe network were shown to generate beta oscillations (a population-level model: Nevado-Holgado et al. 2010; and a model using integrate-and-fire neurons: Kumar et al. 2011). Mathematical analyses of the population-level model revealed conditions the parameters of the STN-GPe model need to satisfy to generate oscillations (Nevado-Holgado et al. 2010; Pavlides et al. 2012; Passillas-Lepine 2013). Second, a computational model of striatum (using Hodgkin-Huxley neurons: McCarty et al. 2011) has been shown to generate beta oscillations. Third, the beta oscillations have been also observed in simulations of the entire cortico-basal-ganglia circuit (a population-level model: van Albada et al. 2009), and the analysis of the model suggested that the beta oscillations originate in the corticothalamic loop in this model.

Additionally, beta oscillations have been also observed in simulations of the entire cortico-basal-ganglia circuit (using integrate-and-fire neurons: Humphries et al. 2006). Furthermore, oscillations close to the beta range (∼12 Hz) were generated in a model of a subset of cortico-basal-ganglia circuit (in which firing rates of individual neurons were described: Leblois et al. 2006). The analysis of the model suggested the oscillations were generated in a loop composed of cortex, STN, output nuclei, and thalamus in this model.

Model-Based Data Analysis

Computational models have been used to infer the changes in network structure occurring in Parkinson’s disease. Eusebio et al. (2009) fitted a simple damped oscillator to event-related potentials recorded from the cortex of Parkinson’s patients after stimulation of STN. They observed that the fitted oscillator had a natural frequency in the beta range, and the data from patients on medications were described by a model with higher damping parameter than data from patients off medications. Also, the dynamic causal modeling was used to infer from local field potentials the differences in effective connectivity in cortico-basal-ganglia-thalamic circuit between healthy and Parkinsonian rats (Moran et al. 2011), and between patients on and off medications (Marreiros et al. 2013). Both of these studies reported increased effective connectivity between the cortex and STN in the states associated with higher beta power.

References

  1. Baker SN, Olivier E, Lemon RN (1997) Coherent oscillations in monkey motor cortex and hand muscle EMG show task-dependent modulation. J Physiol 501(1):225–241PubMedCentralPubMedCrossRefGoogle Scholar
  2. Bevan MD, Magill PJ, Terman D, Bolam JP, Wilson CJ (2002) Move to the rhythm: oscillation in the subthalamic nucleus – external globus pallidus network. Trends Neurosci 25:525–531PubMedCrossRefGoogle Scholar
  3. Brown P (2007) Abnormal oscillatory synchronization in the motor system leads to impaired movement. Curr Opin Neurol 17:656–664CrossRefGoogle Scholar
  4. Brown P, Oliviero A, Mazzone P, Insola A, Tonali P, Di Lazzaro V (2001) Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson’s disease. J Neurosci 21:1033–1038PubMedGoogle Scholar
  5. Chen CC, Litvak V, Gilbertson T, Kuhn A, Lu CS, Lee ST, Tsai CH, Tisch S, Limousin P, Hariz M, Brown P (2007) Excessive synchronization of basal ganglia neurons in 20 Hz slows movement in Parkinson’s disease. Exp Neurol 2015:214–221CrossRefGoogle Scholar
  6. Cruz AV, Mallet N, Magill PJ, Brown P, Averbeck BB (2009) Effects of dopamine depletion on network entropy in the external globus pallidus. J Neurophysiol 102:1092–1102PubMedCentralPubMedCrossRefGoogle Scholar
  7. Engel AE, Fries P (2010) Beta-band oscillations – signalling the status quo? Curr Opin Neurobiol 20:156–165PubMedCrossRefGoogle Scholar
  8. Eusebio A, Pogosyan A, Wang S, Averbeck B, Gaynor LD, Cantiniaux S, Witjas T, Limousin P, Azulay J-P, Brown P (2009) Resonance in subthalamo-cortical circuits in Parkinson’s disease. Brain 132:2139–2150PubMedCentralPubMedCrossRefGoogle Scholar
  9. Hammond C, Bergman H, Brown P (2007) Pathological synchronization in Parkinson’s disease: networks, models and treatments. Trends Neurosci 30:357–464PubMedCrossRefGoogle Scholar
  10. Humphries MD, Stewart RD, Gurney KN (2006) A physiologically plausible model of action selection and oscillatory activity in the basal ganglia. J Neurosci 26:12921–12942PubMedCrossRefGoogle Scholar
  11. Kuhn AA, Kupsch A, Schneider GH, Brown P (2006) Reduction in subthalamic 8–35 Hz oscillatory activity correlates with clinical improvement in PD. Eur J Neurosci 23:1956–1960PubMedCrossRefGoogle Scholar
  12. Kumar A, Cardanobile S, Rotter S, Aertsen A (2011) The role of inhibition in generating and controlling Parkinson’s disease oscillations in the basal ganglia. Front Syst Neurosci 5:86PubMedCentralPubMedCrossRefGoogle Scholar
  13. Leblois A, Boraud T, Meissner W, Bergman H, Hansel D (2006) Competition between feedback loops underlies normal and pathological dynamics in the basal ganglia. J Neurosci 26:3567–3583PubMedCrossRefGoogle Scholar
  14. Mallet N, Pogosyan A, Sharott A, Csicsvari J, Bolam JP, Brown P, Magill PJ (2008a) Disrupted dopamine transmission and the emergence of exaggerated beta oscillations in subthalamic nucleus and cerebral cortex. J Neurosci 28:4795–4806PubMedCrossRefGoogle Scholar
  15. Mallet N, Pogosyan A, Marton LF, Bolam JP, Brown P, Magill PJ (2008b) Parkinsonian oscillations in the external globus pallidus and their relationship with subthalamic nucleus activity. J Neurosci 28:14245–14258PubMedCrossRefGoogle Scholar
  16. Marreiros AC, Cagan H, Moran RJ, Friston KJ, Brown P (2013) Basal ganglia-cortical interactions in Parkinsonian patients. Neuroimage 66:301–310PubMedCentralCrossRefGoogle Scholar
  17. McCarty MM, Moore-Kochlacs C, Gu X, Boyden ES, Han X, Kopell N (2011) Striatal origin of the pathologic beta oscillations in Parkinson’s disease. Proc Natl Acad Sci U S A 108:11620–11625CrossRefGoogle Scholar
  18. Moran R, Mallet N, Litvak V, Dolan RJ, Magill PJ, Friston KJ, Brown P (2011) Alteration in brain connectivity underlying beta oscillations in Parkinsonism. PLoS Comput Biol 7:e1002124PubMedCentralPubMedCrossRefGoogle Scholar
  19. Nevado-Holgado AJ, Terry J, Bogacz R (2010) Conditions for the generation of beta oscillations in the subthalamic nucleus – globus pallidus network. J Neurosci 30:12340–12352CrossRefGoogle Scholar
  20. Passillas-Lepine W (2013) Delay-induced oscillations in Wilson and Cowan’s model: an analysis of the subthalamo-pallidal feedback loop in healthy and Parkinsonian subjects. Biol Cybernet 107: 289–308CrossRefGoogle Scholar
  21. Pavlides A, Hogan SJ, Bogacz R (2012) Improved conditions for the generation of beta oscillations in the subthalamic nucleus-globus pallidus network. Eur J Neurosci 36:2229–2239PubMedCrossRefGoogle Scholar
  22. Plenz D, Kital S (1999) A basal ganglia pacemaker formed by the subthalamic nucleus and external globus pallidus. Nature 400:677–682PubMedCrossRefGoogle Scholar
  23. Pogosyan A, Gaynor LD, Eusebio A, Brown P (2009) Boosting cortical activity at beta-band frequencies slows movement in humans. Curr Biol 19:1637–1641PubMedCentralPubMedCrossRefGoogle Scholar
  24. Rubin JE, Terman D (2004) High frequency stimulation of the subthalamic nucleus eliminates pathological thalamic rhythmicity in a computational model. J Comput Neurosci 16:211–235PubMedCrossRefGoogle Scholar
  25. Tachibana Y, Iwamuro H, Kita H, Takada M, Nambu A (2011) Subthalamo-pallidal interactions underlying parkinsonian neuronal oscillations in the primate basal ganglia. Eur J Neurosci 34:1470–1484PubMedCrossRefGoogle Scholar
  26. Tiesinga P, Sejnowski TJ (2009) Cortical enlightenment: are attentional gamma oscillations driven by ING or PING? Neuron 63:727–732PubMedCentralPubMedCrossRefGoogle Scholar
  27. Van Albada SJ, Gray RT, Drysdale PM, Robinson PA (2009) Mean-field modeling of the basal ganglia-thalamocortical system II. Dynamics of Parkinsonian oscillations. J Theor Biol 257:664–688PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Department of Computer ScienceUniversity of BristolCliftonUK