Basal Ganglia: Beta Oscillations
KeywordsBasal Ganglion Transcranial Magnetic Stimulation Local Field Potential Effective Connectivity Beta Power
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
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.