Deep Brain Stimulation of the Posterior Insula in Chronic Pain: A Theoretical Framework
Abstract
:1. Introduction
2. Neuroanatomical Studies
3. Brain Lesion Studies
4. Functional Imaging Studies
5. Intracranial Recordings during Painful Stimuli
6. Electrical Stimulation of the Insula in Humans
7. Non-Invasive Insular Stimulation in Patients with Chronic Pain
8. Previously Studied DBS Targets for Chronic Pain
9. Conclusions
- First, the optimal electrode target(s) within the insula and landmarks to achieve precise and consistent implantation will require further investigation. The experience gathered by epilepsy surgeons with SEEG implantation in the insula would certainly facilitate their safe and precise positioning. Furthermore, data gathered from intracranial electrical stimulation and recording in epileptic patients have helped to delineate the primary somatosensory region receiving spinothalamic input from the VMPo, most likely to directly affect pain perception [39,44]. Awake surgery with microelectrode recording during painful stimulation or intracranial stimulation would also help refine electrode positioning in the operating room. It would certainly be worthwhile to consider the implantation of additional electrodes in the middle or anterior insula to modulate the affective components of pain, in addition to its somatosensory components.
- Second, the selection of the proper patient population represents a significant challenge. As discussed in Section 4, studies have highlighted abnormal insular activity and connectivity in many chronic pain syndromes. However, chronic pain is an extremely heterogeneous condition, and it remains unclear which patients would most benefit from insular DBS. Fibromyalgia is the pain disorder with the clearer neuroimaging evidence pointing to circuit abnormalities centered on the insula, as the source of sensory and affective hypersensitivity to external and interoceptive stimuli [26]. However, the heterogeneity of the syndrome and its psychiatric comorbidities represent major challenges. Patients with fibromyalgia can be expected to be more sensitive to post-operative pain from the insertion of the electrode and battery. Demonstration of cost-effectiveness in a syndrome that carries important negative bias and misunderstanding in the general population and medical community might also prove challenging. Other promising patient populations include central neuropathic pain from stroke or spinal cord damage, complex regional pain syndrome, and post-amputation phantom pain. Whatever the source of chronic pain, patients will need to be managed at a tertiary-care chronic pain clinic, fail all conventional treatments, and have symptoms severe and incapacitating enough to justify the invasiveness and cost of DBS as a last-resort therapy.
- Third, there is little data from which to infer the potential effects of electrical stimulation of the posterior insula on the activity of pain networks or to infer which stimulation parameters would be most effective. Low-frequency stimulation of the posterior insula was shown to elicit pain [39], and high-frequency stimulation was shown to transiently increase temperature pain thresholds [43]. The exact neural mechanisms underlying these effects are currently unknown. Initially, since the clinical response elicited by high-frequency stimulation was similar to a lesion of the same region (for instance, the subthalamic nucleus), high-frequency stimulation was thought to functionally inactivate the neuronal bodies, from depolarization blockade and/or neurotransmitter depletion [136]. We have since understood that DBS pulses are propagated to anatomically connected regions by orthodromic and antidromic action potentials generated in axons in the vicinity of the target region, including afferents and efferents of the target, as well as nearby passing fibers [136]. DBS also modifies the neurotransmitter environment by its effect on astrocytes [136]. We currently do not have the neuroanatomical or computational knowledge to predict the effect of localized electrical stimulation on the activity of multiregional brain networks, although this is the subject of an ongoing investigation [137]. It is equally difficult to predict which stimulation parameters would better re-establish proper neuronal activity within the insular network. Based on preliminary evidence with high-frequency insula stimulation (150 Hz) [43] and experience with DBS of the ACC (130 Hz, 450 μs) [123], a region with a baseline neurophysiology that is similar to the insula [138], we intend to use an initial stimulation frequency of 130 Hz. The use of a sensing-enabled DBS system will help to better understand the effect of different stimulation parameters on insular neurophysiology.
- Fourth, regarding the intensity of stimulation, the risk of stimulation-induced seizure is an important concern. The insula is well known to be an epileptogenic structure [139], and non-invasive stimulation of the insula was shown to trigger partial insular seizure in a recent study [104]. DBS of the ACC—another well-known epileptogenic region—has also triggered partial seizures in some patients when stimulation intensity was increased too quickly, including continuing epilepsy after electrode removal in a patient [126]. To lower the risk of stimulation-induced seizure and better refine stimulation intensity throughout the day, the use of a sensing-enabled DBS system would be desirable [140]. Stimulation with the cycle mode, rather than prolonged continuous stimulation, has also been proposed to reduce the risk of seizures [140,141]. Moreover, subjective experience of pain varies throughout the day, and hence, there would be a possibility to modulate stimulation according to the sensing of brain activity—in other words, closed-loop stimulation [142]. In this regard, an important challenge will be to develop reliable, real-time decoders of the subjective pain state based on intracranial recordings. This is the subject of ongoing efforts by different research teams [142].
- Fifth, the outcome measures of insular DBS will require thoughtful considerations. Of course, pain ratings on the visual analog scale, quality-of-life ratings, pain interference with daily activities, mood, medication use, and cortical electrophysiology measurements will represent important outcome measures. Appropriate trial designs with sham stimulation groups will be of utmost importance, given the high risk of the placebo effect. Finally, it will be important to monitor the persistence of the effect over time, as previous trials of DBS for chronic pain with other target regions have all shown initially encouraging results, which proved only temporary over time in most patients [4,11].
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Acknowledgments
Conflicts of Interest
References
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Bergeron, D.; Obaid, S.; Fournier-Gosselin, M.-P.; Bouthillier, A.; Nguyen, D.K. Deep Brain Stimulation of the Posterior Insula in Chronic Pain: A Theoretical Framework. Brain Sci. 2021, 11, 639. https://doi.org/10.3390/brainsci11050639
Bergeron D, Obaid S, Fournier-Gosselin M-P, Bouthillier A, Nguyen DK. Deep Brain Stimulation of the Posterior Insula in Chronic Pain: A Theoretical Framework. Brain Sciences. 2021; 11(5):639. https://doi.org/10.3390/brainsci11050639
Chicago/Turabian StyleBergeron, David, Sami Obaid, Marie-Pierre Fournier-Gosselin, Alain Bouthillier, and Dang Khoa Nguyen. 2021. "Deep Brain Stimulation of the Posterior Insula in Chronic Pain: A Theoretical Framework" Brain Sciences 11, no. 5: 639. https://doi.org/10.3390/brainsci11050639