A putative generalized model of the effects and mechanism of action of High Frequency Electrical Stimulation of the Central Nervous System
Identifieur interne : 002D97 ( Main/Exploration ); précédent : 002D96; suivant : 002D98A putative generalized model of the effects and mechanism of action of High Frequency Electrical Stimulation of the Central Nervous System
Auteurs : Alim-Louis Benabid [France] ; Bradley Wallace [France] ; John Mitrofanis [France] ; Rong Xia [France] ; Brigitte Piallat [France] ; Stephan Chabardes [France] ; Francois Berger [France]Source :
- Acta neurologica belgica [ 0300-9009 ] ; 2005.
Descripteurs français
- Pascal (Inist)
English descriptors
- KwdEn :
Abstract
High-frequency stimulation (HFS) of neural structures has been used since 1997 as an alternative to lesions in functional neurosurgery of movement disorders, and more recently, it has been applied to the treatment of epilepsies, obsessive-compulsive disorders, cluster headaches, and has other applications in experimental models, particularly for obesity. Although their clinical efficacy is not questioned, and that the effects most of the time parallel those of ablative techniques, leading to the concept of functional inhibition, the intimate mechanisms by which HFS induces excitation within fiber bundles and seems to inhibit cellular nuclei is still strongly debated. Principally due to the observation of long-term clinical effects over a period up to 15 years, it is clear that the mechanism is not due to a progressive lesion, as at every moment the interruption of stimulation reverses totally the effects. There is no current proof that long-term HFS is able to reset neural networks, or to induce profound modifications of the functional organization or of the synaptic connectivity. To understand what is responsible for the immediate, reversible and adaptable effects of HFS, several mechanisms must be considered, which might be involved simultaneously or in sequence : i) Jamming of neural transmission through stimulated nuclei is one possibility, based on the principle that the regular imposed activity might drive the neurons to fire in a regular pattern, making it impossible to transmit more subtle messages, either normal or abnormal. Although it is difficult to prove this type of mechanism, it might account for the reports of increased activity following HFS in various structures. ii) Direct inhibition of spike initiation at the level of the membrane could be due to activation of inhibitory terminals, particularly gaba-ergic, or by a blockade of the voltage gated ion channels. iii) Recent data show that HFS decreases the production and release of low molecular weight proteic neurotransmitters, which could account for the functional inhibition while the efferent axon is still excited by the electrical stimulus. iv) Retrograde activation of upstream neuronal structures, as reported in the external pallidum during stimulation of STN, might be responsible of additional jamming-like effects due to collisions with descending spikes. Due to the geometry of the chronic electrodes used in human patients, and to their size as compared to the size of the neural elements, the tentative model of the mechanisms of HFS must take into account possible simultaneous effects of stimulation on the presynaptic, synaptic, axonal, dendritic and post synaptic events, as well as on the fibers "de passage" involved in the vicinity of the stimulating electrodes. To this respect, modeling of the spatial distribution of voltages and currents appears to be of extreme importance. A global model of the mechanism of HFS is proposed. At the level of the somata and cell bodies, spike initiation is profoundly altered leading to a total suppression of spikes, as recorded in pallidal and subthalamic neurons of parkinsonian patients, possibly alterning with intensity driven spike activity, such as reported in STN on brain slices, using intracellular recordings. It seems from these studies that the presynaptic effects are not the determining events.
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<keywords scheme="Pascal" xml:lang="fr"><term>Système nerveux pathologie</term>
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<front><div type="abstract" xml:lang="en">High-frequency stimulation (HFS) of neural structures has been used since 1997 as an alternative to lesions in functional neurosurgery of movement disorders, and more recently, it has been applied to the treatment of epilepsies, obsessive-compulsive disorders, cluster headaches, and has other applications in experimental models, particularly for obesity. Although their clinical efficacy is not questioned, and that the effects most of the time parallel those of ablative techniques, leading to the concept of functional inhibition, the intimate mechanisms by which HFS induces excitation within fiber bundles and seems to inhibit cellular nuclei is still strongly debated. Principally due to the observation of long-term clinical effects over a period up to 15 years, it is clear that the mechanism is not due to a progressive lesion, as at every moment the interruption of stimulation reverses totally the effects. There is no current proof that long-term HFS is able to reset neural networks, or to induce profound modifications of the functional organization or of the synaptic connectivity. To understand what is responsible for the immediate, reversible and adaptable effects of HFS, several mechanisms must be considered, which might be involved simultaneously or in sequence : i) Jamming of neural transmission through stimulated nuclei is one possibility, based on the principle that the regular imposed activity might drive the neurons to fire in a regular pattern, making it impossible to transmit more subtle messages, either normal or abnormal. Although it is difficult to prove this type of mechanism, it might account for the reports of increased activity following HFS in various structures. ii) Direct inhibition of spike initiation at the level of the membrane could be due to activation of inhibitory terminals, particularly gaba-ergic, or by a blockade of the voltage gated ion channels. iii) Recent data show that HFS decreases the production and release of low molecular weight proteic neurotransmitters, which could account for the functional inhibition while the efferent axon is still excited by the electrical stimulus. iv) Retrograde activation of upstream neuronal structures, as reported in the external pallidum during stimulation of STN, might be responsible of additional jamming-like effects due to collisions with descending spikes. Due to the geometry of the chronic electrodes used in human patients, and to their size as compared to the size of the neural elements, the tentative model of the mechanisms of HFS must take into account possible simultaneous effects of stimulation on the presynaptic, synaptic, axonal, dendritic and post synaptic events, as well as on the fibers "de passage" involved in the vicinity of the stimulating electrodes. To this respect, modeling of the spatial distribution of voltages and currents appears to be of extreme importance. A global model of the mechanism of HFS is proposed. At the level of the somata and cell bodies, spike initiation is profoundly altered leading to a total suppression of spikes, as recorded in pallidal and subthalamic neurons of parkinsonian patients, possibly alterning with intensity driven spike activity, such as reported in STN on brain slices, using intracellular recordings. It seems from these studies that the presynaptic effects are not the determining events.</div>
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