Elsevier

Neurologic Clinics

Volume 38, Issue 1, February 2020, Pages 201-214
Neurologic Clinics

Neuroimaging of Deep Brain Stimulation

https://doi.org/10.1016/j.ncl.2019.09.005Get rights and content

Section snippets

Key points

  • Advances in functional neurosurgery were supported in the last decade by modern imaging and innovations in neurotechnology.

  • DBS targeting changed from indirect targeting by the technical advancement of MRI technology to direct targeting.

  • DTI of white matter fibers helps to understand the effect of DBS, improves surgical outcome, and became an imaging tool in human translational neuroscience.

  • Parcellation of cortical and subcortical structures let functional neurosurgeons get detailed functional

Introduction of tailored MRI techniques in surgical planning

To increase optimal placement of DBS electrodes several MRI sequences have been introduced to achieve more precise targeting, and advancements in magnetic field strength have also resulted in higher resolution images. The introduction of proton density imaging provides high contrast rate between the intramedullary lamina and the intranuclear gray, making it possible to distinguish between the internal part of the globus pallidus (GPi) and external part of the globus pallidus, making the

Advancements in movement disorders

Since the first implantation carried out by Benabid and coworkers19 several advancements have occurred to take DBS surgery in movement disorders several steps further from its infancy. Ventriculography and the use of standard coordinates have been replaced by modern MRI and individually tailored therapeutic plans. Not only has the targeting been refined, but robot-assisted procedures have also been introduced to achieve the best clinical outcome (Fig. 3).20,21

Clinical rationale of the stereotactic targets in movement disorders

The three main therapeutic targets (the internal part of the GPi, the ventral intermediate nucleus [VIM], and the STN) where in the center of constant debates between clinicians and researchers because each provides certain benefits for patients after electrode implantation in PD, DT, or essential tremor. For example, although VIM stimulation can achieve significant benefit in tremor-dominant PD or essential tremor, it only has moderately sufficient long-term impact on rigidity and none on

The role of connectivity patterns and diffusion tensor imaging in movement disorders

Although proper visualization of the STN, the GPi or the VIM is crucial to achieve the best clinical results, several centers still favor intraoperative electrophysiology during implantation to maintain an optimal target point within the microstructure of the nuclei.25,26 Recent studies have emphasized that the STN, the GPi, and the VIM all connect to distinct cortical areas, which can explain unwanted side effects observed in, for example, ventromedial STN stimulation. Most optimal results in

Deep brain stimulation for epilepsy

One-third of the population of the 66 million epilepsy patients worldwide suffer from drug-resistant epilepsy. Those who have focal seizures or focal lesions are good candidates for resective surgery. Those who are neither successfully treated by drugs and ketogenic diet nor optimal candidates for resective surgery are potential candidates for neuromodulation. Neuromodulation of epilepsy could be noninvasive or invasive. The invasive neuromodulative techniques could stimulate peripheral nerves,

Deep brain stimulation for psychiatric indications

The Austrian physician Gottlieb Burckhardt was the first to pioneer neurosurgical intervention, in the form of trephination and topectomy, for psychiatric indications in the late 1880s.56 Although the subsequent presentation of his findings was not well received, this initial work was foundational to the subsequent efforts of Moniz and Lima, beginning in 1935, to introduce the prefrontal leukotomy (commonly known as the frontal lobotomy).57 Rapid popularization of this procedure would come to

An image-based rationale for intervention

The most common psychiatric indication currently explored for surgical intervention is depression. Several intracranial targets have recently been attempted. These include the nucleus accumbens,59 lateral habenula,60 inferior thalamic peduncle,61 ventral capsule/ventral striatum (VC/VS),62 and subgenual cingulate.63 The latter two targets have been explored in randomized controlled trials and are instructive because of a differing basis for exploration. The VC/VS target received a Humanitarian

Contemporary randomized clinical trial results for depression

Based on the previously mentioned open label studies, two separate randomized clinical trials have been recently completed for depression: the RECLAIM (VC/VS)67 and the BROADEN (subgenual cingulate)68 trials. Both trials were terminated before planned enrollment completion. The blind was broken for an interim analysis on the RECLAIM trial following enrollment of 30 out of 208 planned patients. Twenty-nine of 30 patients had completed the blinded phase; there was a 14.3% response rate in the

A connectome-based targeting approach

Throughout the BROADEN study, investigators worked to further tailor the intracranial lead placement targeting strategy that was used. A DTI-based analysis of responders and nonresponders demonstrated a characteristic pattern of connectivity in the vicinity of the active treatment electrode contact. Specifically, responders were observed to have electrode placement at a location representing the confluence of the (1) forceps minor, (2) medial aspect of the uncinate fasciculus, (3) the cingulum

Deep brain stimulation for treatment of chronic pain

Intracranial stimulation for the treatment of chronic pain disorders has been explored in the context of motor cortex stimulation73, 74, 75 and DBS at multiple subcortical targets. DBS targets have included the VS/anterior limb of the interal capsule,76 ventral posterolateral thalamic nucleus,77, 78, 79 periaqueductal/periventricular brainstem nucleus,78 and dorsal anterior cingulate cortex.80,81 DBS was most effective for phantom limb pain, stump pain, failed back surgery syndrome (FBSS),

Summary

Modern imaging opens new advancements for stereotactic and functional neurosurgery. The weaknesses of indirect targeting because of the great individual variability of the patient’s brain became evident. Direct targeting improves accuracy and in DBS surgery can improve outcome. Direct targeting with new MRI sequences and with the MRI-compatible neurotechnological devices allowed comparative analysis for surgical outcome in cases of multicentric studies, which is essential to improve DBS therapy.

Acknowledgments

The authors acknowledge the support of the Hungarian Brain Research Program and the work of Dr László Halász, PhD fellow and neurosurgical resident at Department of Functional Neurosurgery and Center of Neuromodulation, National Institute of Clinical Neurosciences in Budapest.

Disclosure

The authors receives funding from Hungarian Brain Research Program 2017-1.2.1-NKP-2017-00002.

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References (89)

  • C. Lambert et al.

    Confirmation of functional zones within the human subthalamic nucleus: patterns of connectivity and sub-parcellation using diffusion weighted imaging

    Neuroimage

    (2012)
  • S. Little et al.

    The functional role of beta oscillations in Parkinson’s disease

    Parkinsonism Relat Disord

    (2014)
  • W.-J. Neumann et al.

    Long term correlation of subthalamic beta band activity with motor impairment in patients with Parkinson’s disease

    Clin Neurophysiol

    (2017)
  • M.H. Trager et al.

    Subthalamic beta oscillations are attenuated after withdrawal of chronic high frequency neurostimulation in Parkinson’s disease

    Neurobiol Dis

    (2016)
  • H. Akram et al.

    Subthalamic deep brain stimulation sweet spots and hyperdirect cortical connectivity in Parkinson’s disease

    Neuroimage

    (2017)
  • N.M. da Silva et al.

    A diffusion-based connectivity map of the GPi for optimised stereotactic targeting in DBS

    Neuroimage

    (2017)
  • T. Möttönen et al.

    Defining the anterior nucleus of the thalamus (ANT) as a deep brain stimulation target in refractory epilepsy: delineation using 3 T MRI and intraoperative microelectrode recording

    Neuroimage Clin

    (2015)
  • A. Horn et al.

    Lead-DBS v2: towards a comprehensive pipeline for deep brain stimulation imaging

    Neuroimage

    (2019)
  • B.H. Bewernick et al.

    Nucleus accumbens deep brain stimulation decreases ratings of depression and anxiety in treatment-resistant depression

    Biol Psychiatry

    (2010)
  • A. Sartorius et al.

    Deep brain stimulation of the lateral habenula in treatment resistant major depression

    Med Hypotheses

    (2007)
  • D.A. Malone et al.

    Deep brain stimulation of the ventral capsule/ventral striatum for treatment-resistant depression

    Biol Psychiatry

    (2009)
  • H.S. Mayberg et al.

    Deep brain stimulation for treatment-resistant depression

    Neuron

    (2005)
  • D.A. Seminowicz et al.

    Limbic-frontal circuitry in major depression: a path modeling metanalysis

    Neuroimage

    (2004)
  • D.D. Dougherty et al.

    A randomized sham-controlled trial of deep brain stimulation of the ventral capsule/ventral striatum for chronic treatment-resistant depression

    Biol Psychiatry

    (2015)
  • P.E. Holtzheimer et al.

    Subcallosal cingulate deep brain stimulation for treatment-resistant depression: a multisite, randomised, sham-controlled trial

    Lancet

    (2017)
  • P. Riva-Posse et al.

    Defining critical white matter pathways mediating successful subcallosal cingulate deep brain stimulation for treatment-resistant depression

    Biol Psychiatry

    (2014)
  • A.M. Noecker et al.

    StimVision software: examples and applications in subcallosal cingulate deep brain stimulation for depression

    Neuromodulation

    (2018)
  • C.L. McGrath et al.

    Pretreatment brain states identify likely nonresponse to standard treatments for depression

    Biol Psychiatry

    (2014)
  • V. Abreu et al.

    Thalamic deep brain stimulation for neuropathic pain: efficacy at three years’ follow-up

    Neuromodulation

    (2017)
  • S.G.J. Boccard et al.

    Deep brain stimulation for chronic pain

    J Clin Neurosci

    (2015)
  • S.G.J. Boccard et al.

    Long-term results of deep brain stimulation of the anterior cingulate cortex for neuropathic pain

    World Neurosurg

    (2017)
  • J. Maarrawi et al.

    Brain opioid receptor density predicts motor cortex stimulation efficacy for chronic pain

    Pain

    (2013)
  • H. Sims-Williams et al.

    Deep brain stimulation of the periaqueductal gray releases endogenous opioids in humans

    Neuroimage

    (2017)
  • S.L. Owen et al.

    Pre-operative DTI and probabilisitic tractography in four patients with deep brain stimulation for chronic pain

    J Clin Neurosci

    (2008)
  • T.E.J. Behrens et al.

    Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging

    Nat Neurosci

    (2003)
  • D. Dormont et al.

    Is the subthalamic nucleus hypointense on T2- weighted images? A correlation study using MR imaging and stereotactic atlas data

    AJNR Am J Neuroradiol

    (2004)
  • A. Schäfer et al.

    Direct visualization of the subthalamic nucleus and its iron distribution using high-resolution susceptibility mapping

    Hum Brain Mapp

    (2012)
  • M.E. Ryan

    Utility of double inversion recovery sequences in MRI

    Pediatr Neurol Briefs

    (2016)
  • M.P. Wattjes et al.

    Double inversion recovery brain imaging at 3T: diagnostic value in the detection of multiple sclerosis lesions

    AJNR Am J Neuroradiol

    (2007)
  • S. Jbabdi et al.

    Model-based analysis of multishell diffusion MR data for tractography: how to get over fitting problems

    Magn Reson Med

    (2012)
  • B. Jeurissen et al.

    Probabilistic fiber tracking using the residual bootstrap with constrained spherical deconvolution

    Hum Brain Mapp

    (2011)
  • J.-D. Tournier et al.

    MRtrix: diffusion tractography in crossing fiber regions

    Int J Imaging Syst Technol

    (2012)
  • A. Leemans et al.

    Mathematical framework for simulating diffusion tensor MR neural fiber bundles

    Magn Reson Med

    (2005)
  • M. Hernández et al.

    Accelerating fibre orientation estimation from diffusion weighted magnetic resonance imaging using GPUs

    PLoS One

    (2013)
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    • Neuroimaging and electrophysiology meet invasive neurostimulation for causal interrogations and modulations of brain states

      2020, NeuroImage
      Citation Excerpt :

      In this view, modern brain imaging has the ability to increase DBS efficacy and reduce adverse effects reported to be associated with suboptimal placement of electrode contacts (Rolston et al., 2016; Wodarg et al., 2012), possibly optimizing a patient’s long-term therapeutic outcome. Preoperatively, structural brain imaging can robustly predict postoperative outcomes across diseases and can, thus, be further implemented for improved selection of those patients who are candidates for DBS intervention (Eross et al., 2020; Gonzalez-Escamilla et al., 2019; Muthuraman et al., 2017). This information can also be used as exclusion criteria for patients who would likely not benefit from DBS therapy (Gonzalez-Escamilla et al., 2019).

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