Deep brain stimulation programming: mechanisms, principles, and practice
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Most specifically, increased beta oscillations Hz are observed in cortico-basal ganglia circuits in PD Brown et al. According to Mallet et al. In terms of functional role, a correlation between beta band power in STN local field potentials LFP and bradykinesia and rigidity has been established Davidson et al. In addition, a correlation between BG oscillations in the theta band Hz and limb tremor has been established in PD patients Davidson et al. Both theta and beta oscillations are thought to be antikinetic Brown, ; Hutchison et al.
In contrast, gamma band oscillatory activities Hz , thought to be prokinetic, are less prominent in the BG and cortex of PD patients and in PD animal models Wang et al. It has been shown that administration of levodopa restores gamma band activity while beta band power is suppressed, which is paralleled by improvements in motor symptoms Brown, ; Gatev et al. The experiments of Costa et al.
DBS applied at frequencies below 60 Hz were found to have no clinical effect, or even to deteriorate PD symptoms and worsen motor performance Rizzone et al. Initially, since DBS showed similar therapeutic benefits as surgical lesions, it was hypothesized that the effective mechanism of DBS was either based on synaptic inhibition or on depolarization blockade Breit et al. DBS affects indifferently multiple neural elements, including myelinated and unmyelinated axons, dendrites, and cell bodies, which may be differentially activated see Section 3.
Extracellular stimulation may excite or block axons of passage, and fiber activation will result in both antidromic and orthodromic propagation Chiken and Nambu, ; Hashimoto et al. However, due to the presence of significant stimulation artefacts, it is complicated to identify the activity patterns occurring during STN stimulation from simultaneous recordings in STN or neighbouring structures. Therefore, the responses following short bursts of stimulation are used to analyze local and global stimulation effects.
Book: Deep Brain Stimulation Programming: Mechanisms, Principles and Practice - Neurosurgery
A new promising method in experimental research is the use of optogenetics: light can be used to target individual neurons that have been genetically modified such that they express light-sensitive ion channels, allowing their precise activation and inactivation. With this technique, Gardinaru et al. In conclusion, the effects of DBS appear much more complex than a simple inhibition of the targeted structure, which has become apparent in part through modeling efforts.
An abundance of computational models has been developed in an attempt to explain the role of part of the BG-thalamo-cortical loop in health and disease, which also may aid in understanding the mechanism s of DBS. These models provide pieces of information regarding the seemingly contradictory effect that increased GPi firing associated with PD should require high-frequency stimulation supposedly enhancing GPi inhibitory output even further to improve motor symptoms.
The starting point for modeling is often based on the interpretation given to BG function and the neuronal mechanism s underlying PD symptoms. Since a consensus is still to be reached regarding BG function, inherently different approaches have been chosen, resulting in computational models differing in a number of ways.
A selection of models is described in this review. In order to model the changes that are observed in the firing patterns in the pathological BG compared to the physiological patterns, neuronal activity may be investigated at the neuronal level, based on neurophysiological and neuroanatomical data. Such models consist of single neurons that are represented by a system of equations describing membrane dynamics see the seminal work by Hodgkin and Huxley, , which has been used in hundreds of models since then.
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In these models, action potentials are generated by the opening and closing of ion channels, as in biological neurons, with each type of ion channel having its own dynamics in terms of the extent and rate of opening and closing. An important issue that has extensively been investigated using these types of models is whether brain rhythms are caused by single cells having pacemaker properties Lopes da Silva, This issue is relevant in describing normal as well as pathological neuronal behaviour, such as synchronized oscillations.
As suggested by several research groups, low frequency oscillations Hz associated with PD may originate in the BG Brown, and cortex Terman et al. The suggested mechanism behind these sustained, low-frequency oscillations of the STN-GPe network was that excitatory STN output leads to GPe bursting, sequentially leading first to hyperpolarization and then rebound bursting in the STN, initiating a new cycle by inducing GPe bursting activity Plenz and Kital, ; Holgado et al.
Under physiological conditions, GPi output is irregular and uncorrelated, allowing the thalamus to transmit faithfully excitatory sensorimotor inputs to cortical areas. In the model, it was shown that increased striatal input to, and weakened intrapallidal inhibition within, the indirect pathway as included in the model switched BG global activity from irregular to rhythmic, resembling the parkinsonian state consistent with experimental data DeLong, ; Filion and Tremblay, ; Wichmann et al.
It was shown that GPi model neurons fired bursts of action potentials at a frequency of Hz i. This results in phasic inhibition of TC cells, which are no longer able to transmit cortical input faithfully. Applying DBS at high frequency Hz in the model as an excitatory input to all STN neurons, resulted in GPi neurons to tonically fire at high frequency, therewith eliminating the oscillatory nature of TC cell inhibition and restoring the ability of TC cells to relay sensorimotor input Rubin and Terman, ; Heida et al.
Using a slightly modified version of the TC cell model, it was tested how different patterns of GPi inhibition, generated from experimental recordings of physiological and parkinsonian monkeys with and without DBS, affected TC relay fidelity Guo et al. This study showed that, without DBS, TC relay fidelity was compromised when receiving input recorded from the GPi of a parkinsonian monkey compared to the GPi activity recorded from a healthy monkey. Relay fidelity improved significantly under therapeutic DBS conditions, but not under sub-therapeutic conditions.
Clinical observations indicate that PD motor symptoms are still present for therapeutic stimulation frequencies at sub-therapeutic amplitudes. By assuming that DBS does not completely replace oscillatory synchronous activity in the STN, stimulus amplitude effects can be analyzed Cagnan et al. Meijer et al. Without additional sensorimotor input i. This pathological activity can be stopped by cortical excitatory input, which may be associated with the execution of voluntary movements resting tremor is usually absent during voluntary movement.
Low-frequency DBS enhances rebound bursts, while high-frequency DBS with amplitudes above a certain threshold level may suppress those bursts. Excessive amplitudes, however, may block the relay of excitatory input, suggesting that DBS effectiveness consists of diminishing rebound activity while preserving the relay function. This results in a clinically effective stimulation window that requires high amplitudes for stimulation frequencies below 40 Hz, in comparison to stimulation frequencies above 70 Hz.
This is in accordance with the observed inverse relationship between therapeutic stimulation frequency and amplitude Benabid et al. The complexity of multi-compartment single-cell models requires large amounts of computational power. Cagnan et al. Interestingly, they found no mismatch between the two, suggesting that the dendritic structure as included in the multi-compartment model did not have a significant effect on the main functioning of the TC cells with regard to the conditions tested.
A next step in reducing model dimensions of the STN-GPe network models is the use of a mean-field approach the activity of each structure being described by a distribution of membrane voltages; see also the next section on neural mass models and incorporating STN-GPe connectivity patterns derived from neuroanatomy.
Modolo et al. As in the Rubin and Terman model , switching from physiological STN-GPe activity to pathological, low-frequency oscillations characteristic of PD was modelled by increased striatal input to the GPe. It was suggested that, at high DBS frequencies, STN neurons only evoked subthreshold responses due to their inability to follow DBS pulses, thereby leading to a suppression of low-frequency oscillations.
The possibility that DBS provides clinical improvements by restoring functional relay of sensorimotor inputs by TC cells, as described in this and the previous section, may be plausible. The fact that lesioning as well as application of DBS in the Vim provide clinical improvements in PD tremor may prove that cerebellar instead of BG pathways may be involved in tremor generation since BG does not project to the Vim Bostan et al. Furthermore, it questions the hypothesis that restoring the thalamic relay of sensorimotor inputs is involved in DBS therapeutic effects.
Deep Brain Stimulation Programming: Mechanisms, Principles and Practice
Novel targets and stimulation paradigms have been tested by Kumar et al. GPe stimulation was tested by injecting Poisson types of inhibitory input of varying frequencies to a selection of GPe neurons for 20 ms. A stimulation-induced increase in the firing rate of GPe neurons was found to be effective in reducing pathological oscillations.
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Furthermore, two methods of periodic stimulation were implemented: 1 Excitatory inputs to STN were periodically switched on and off at a frequency in the range of 10 to Hz , which is equivalent to repeated electrical stimulation of excitatory afferents to the STN resulting in a cessation of axonal spiking due to adaption effects. Only frequencies above Hz appeared to be effective.
This type of stimulation was found to be more effective in quenching pathological oscillations than periodic stimulation. In addition to the question of whether alternative DBS patterns would be equally, or even more, effective in alleviating PD symptoms, we may also wonder whether certain stimulation patterns would be effective in patients who do not respond effectively to standard, high-frequency DBS. In a computational model of the parkinsonian BG, several non-regular patterns of DBS, all having a mean frequency of Hz, but having non-regular features such as short periods in which pulses were absent or presence of short bursts of pulses, were found to suppress beta band oscillatory activity Brocker et al.
The degree of suppression in the model was strongly correlated with the clinical efficacy across stimulation patterns as tested during a finger tapping task. Another recent study investigated the possibility of using irregular stimulation patterns instead of the standard high-frequency stimulation pattern classically used in DBS Summerson et al.
These authors used a stochastic stimulation period, keeping the average stimulation frequency constant. Interestingly, both in their model and in a rat model of PD 6-OHDA , they found that stochastic DBS resulted in an inter-spike interval ISI entropy decrease, along with a decrease in beta band power classically linked with an improvement in PD motor symptoms. However, these results are in contradiction with other studies as mentioned and replicated by McConnell et al.
Instead of using a single target for stimulation, it has been suggested to use multiple sites for stimulation Hauptmann et al.
Table of Contents
Since PD symptoms are associated with hyper-synchronized pathological neuronal activity, it may be assumed that effective stimulation paradigms should aim at desynchronizing hyper-synchronized networks. DBS Books:. This site uses Akismet to reduce spam. Learn how your comment data is processed. Your credit card will not be charged until we ship the item. Like this: Like Loading Patients with inactivated stimulation DBS-OFF showed an increase in syllable duration when compared with an age-matched group of healthy control speakers. However, numerically there was a trend for patients to exhibit larger proportions of instances with voicing-during-closure 0.
All three POAs showed the same pattern numerically, i. Articulatory results Table 4 presents the results for the articulatory variables describing the consonantal gesture, 5 duration of the acceleration phase, 6 duration of the deceleration phase, 7 maximum displacement, 8 peak velocity, and 9 stiffness, across subjects for the three different groups, sorted by POA. Table 4. Fig 7. Fig 8. Fig 9. Order effects of phenotypical assessments EMA recordings were made after stimulation changes had been kept constant for a minimum of 20 minutes.