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Mapping autonomic, mood and cognitive effects of hypothalamic region deep brain stimulation.

ABSTRACT: Because of its involvement in a wide variety of cardiovascular, metabolic and behavioural functions, the hypothalamus constitutes a potential target for neuromodulation in a number of treatment-refractory conditions. The precise neural substrates and circuitry subserving these responses, however, are poorly characterized to date. We sought to retrospectively explore the acute sequelae of hypothalamic region deep brain stimulation and characterize their neuroanatomical correlates. To this end we studied-at multiple international centres-58 patients (mean age: 68.5 ± 7.9 years, 26 females) suffering from mild Alzheimer's disease who underwent stimulation of the fornix region between 2007 and 2019. We catalogued the diverse spectrum of acutely induced clinical responses during electrical stimulation and interrogated their neural substrates using volume of tissue activated modelling, voxel-wise mapping, and supervised machine learning techniques. In total 627 acute clinical responses to stimulation-including tachycardia, hypertension, flushing, sweating, warmth, coldness, nausea, phosphenes, and fear-were recorded and catalogued across patients using standard descriptive methods. The most common manifestations during hypothalamic region stimulation were tachycardia (30.9%) and warmth (24.6%) followed by flushing (9.1%) and hypertension (6.9%). Voxel-wise mapping identified distinct, locally separable clusters for all sequelae that could be mapped to specific hypothalamic and extrahypothalamic grey and white matter structures. K-nearest neighbour classification further validated the clinico-anatomical correlates emphasizing the functional importance of identified neural substrates with area under the receiving operating characteristic curves between 0.67 and 0.91. Overall, we were able to localize acute effects of hypothalamic region stimulation to distinct tracts and nuclei within the hypothalamus and the wider diencephalon providing clinico-anatomical insights that may help to guide future neuromodulation work.

SUBMITTER: Neudorfer C

PROVIDER: S-EPMC8557336 | biostudies-literature | 2021 Oct

REPOSITORIES: biostudies-literature

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Mapping autonomic, mood and cognitive effects of hypothalamic region deep brain stimulation.

Neudorfer Clemens C Elias Gavin J B GJB Jakobs Martin M Boutet Alexandre A Germann Jürgen J Narang Keshav K Loh Aaron A Paff Michelle M Horn Andreas A Kucharczyk Walter W Deeb Wissam W Salvato Bryan B Almeida Leonardo L Foote Kelly D KD Rosenberg Paul B PB Tang-Wai David F DF Anderson William S WS Mari Zoltan Z Ponce Francisco A FA Wolk David A DA Burke Anna D AD Salloway Stephen S Sabbagh Marwan N MN Chakravarty M Mallar MM Smith Gwenn S GS Lyketsos Constantine G CG Okun Michael S MS Lozano Andres M AM

Brain : a journal of neurology 20211001 9

Because of its involvement in a wide variety of cardiovascular, metabolic and behavioural functions, the hypothalamus constitutes a potential target for neuromodulation in a number of treatment-refractory conditions. The precise neural substrates and circuitry subserving these responses, however, are poorly characterized to date. We sought to retrospectively explore the acute sequelae of hypothalamic region deep brain stimulation and characterize their neuroanatomical correlates. To this end we ...[more]

PMID: 33905474

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Project description:BackgroundDeep brain stimulation (DBS) has been successfully used for the treatment of circuitopathies including movement, anxiety, and behavioral disorders. The hypothalamus is a crucial integration center for many peripheral and central pathways relating to cardiovascular, metabolic, and behavioral functions and constitutes a potential target for neuromodulation in treatment-refractory conditions. To conduct a systematic review, investigating hypothalamic targets in DBS, their indications, and the primary clinical findings.MethodsPubMed, Scopus, and Web of Science databases were searched in accordance with the PRISMA guideline to identify papers published in English studying DBS of the hypothalamus in humans.ResultsAfter screening 3,148 papers, 34 studies consisting of 412 patients published over two decades were included in the final review. Hypothalamic DBS was indicated in refractory headaches (n = 238, 57.8%), aggressive behavior (n = 100, 24.3%), mild Alzheimer's disease (n = 58, 14.1%), trigeminal neuralgia in multiple sclerosis (n = 5, 1.2%), Prader-Willi syndrome (n = 4, 0.97%), and atypical facial pain (n = 3, 0.73%). The posterior hypothalamus was the most common DBS target site across 30 studies (88.2%). 262 (63.6%) participants were males, and 110 (26.7%) were females. 303 (73.5%) patients were adults whereas 33 (8.0%) were pediatrics. The lowest mean age of participants was 15.25 ± 4.6 years for chronic refractory aggressiveness, and the highest was 68.5 ± 7.9 years in Alzheimer's disease patients. The mean duration of the disease ranged from 2.2 ± 1.7 (mild Alzheimer's disease) to 19.8 ± 10.1 years (refractory headaches). 213 (51.7%) patients across 29 studies (85.3%) reported symptom improvements which ranged from 23.1% to 100%. 25 (73.5%) studies reported complications, most of which were associated with higher voltage stimulations.ConclusionsDBS of the hypothalamus is feasible in selected patients with various refractory conditions ranging from headaches to aggression in both pediatric and adult populations. Future large-scale studies with long-term follow-up are required to validate the safety and efficacy data and extend these findings.

Project description:Following its introduction in 2014 and with support of a broad international community, the open-source toolbox Lead-DBS has evolved into a comprehensive neuroimaging platform dedicated to localizing, reconstructing, and visualizing electrodes implanted in the human brain, in the context of deep brain stimulation (DBS) and epilepsy monitoring. Expanding clinical indications for DBS, increasing availability of related research tools, and a growing community of clinician-scientist researchers, however, have led to an ongoing need to maintain, update, and standardize the codebase of Lead-DBS. Major development efforts of the platform in recent years have now yielded an end-to-end solution for DBS-based neuroimaging analysis allowing comprehensive image preprocessing, lead localization, stimulation volume modeling, and statistical analysis within a single tool. The aim of the present manuscript is to introduce fundamental additions to the Lead-DBS pipeline including a deformation warpfield editor and novel algorithms for electrode localization. Furthermore, we introduce a total of three comprehensive tools to map DBS effects to local, tract- and brain network-levels. These updates are demonstrated using a single patient example (for subject-level analysis), as well as a retrospective cohort of 51 Parkinson's disease patients who underwent DBS of the subthalamic nucleus (for group-level analysis). Their applicability is further demonstrated by comparing the various methodological choices and the amount of explained variance in clinical outcomes across analysis streams. Finally, based on an increasing need to standardize folder and file naming specifications across research groups in neuroscience, we introduce the brain imaging data structure (BIDS) derivative standard for Lead-DBS. Thus, this multi-institutional collaborative effort represents an important stage in the evolution of a comprehensive, open-source pipeline for DBS imaging and connectomics.

Project description:ObjectiveHypothalamic dysfunction may result in morbid obesity as a consequence of decreased energy expenditure, decreased feelings of satiety, and increased fat storage. In patients with hypothalamic dysfunction, neurobehavioral dysfunction is also often present. Currently, no effective treatment has been found for hypothalamic obesity (HO). We hypothesize that deep brain stimulation (DBS) may be an effective treatment for patients with hypothalamic dysfunction, aiming to treat HO as well as the neurobehavioral dysfunction.MethodsA systematic search was conducted in the PubMed, EMBASE and Cochrane Library databases for studies published until May 2022 reporting on DBS for the treatment of HO.ResultsThree studies met the predetermined inclusion criteria, with in total six patients treated with DBS for HO, of which five patients with Prader-Willi syndrome (PWS) and one patient with HO after treatment for craniopharyngioma (CP). Targets of DBS included the lateral hypothalamic area (LHA) and the nucleus accumbens (NAcc). In patients with PWS, LHA-DBS was associated with a mean increase of Body Mass Index (BMI) (+5.8%), with no change in hormonal levels, results of blood workup, sleep, or neuropsychological evaluation. In the patient with CP, NAcc-DBS was associated with a decrease in BMI (-8.7%) and a subjective increase in mental health, energy and willingness to act, and no feeling of increased appetite. No objective measurements on neurobehavioral function were reported. No severe adverse events were reported in these cases. Mild to moderate adverse events included hypomanic symptoms and infection. All patients with a described follow-up period (n = 5) were able to sustain the treatment for at least 6 months with few interruptions.ConclusionThere is limited research reporting on DBS for HO. The effectiveness differed across studies and the evidence is limited. Although there may be potential for DBS treatment in the severe-refractory condition of HO in patients with CP, more research is needed for target selection and evaluation of effectiveness.

Project description:Changes in personality are one of the main concerns Parkinson's disease (PD) patients raise when facing the decision to undergo neurosurgery for deep brain stimulation (DBS) of the subthalamic nucleus (STN). While clinical instruments for monitoring functional changes following DBS surgery are well-established in the daily therapeutic routine, personality issues are far less systematically encompassed. Moreover, while sex disparities in the outcomes of STN-DBS therapy have been reported, little is known about the different effects that DBS treatment may have on mood and personality traits in female and male patients. To this aim, the effect of STN-DBS on personality traits was assessed in 46 PD patients (12 women and 34 men) by means of the Freiburg Personality Inventory. The Becks Depression Inventory (BDI-I) and the Parkinson's Disease Questionnaire were used to evaluate patients' level of depression and quality of life (QoL). Patients completed the questionnaires a few days before, within the first year, and 2 years after surgery. The 12 personality traits defined by the FPI-R questionnaire did not change significantly after STN-DBS surgery (p = 0.198). Women declared higher depression scores through all study stages (p = 0.009), but also showed a stronger QoL amelioration after surgery than male patients (p = 0.022). The BDI-I scores of female patients clearly correlated with their levodopa equivalent daily dose (LEDD; r = 0.621, p = 0.008). Remarkably, in both male and female patients, higher pre-operative LEDDs were related to worse post-operative QoL scores (p = 0.034). These results mitigate the concerns about systematic personality changes due to STN-DBS treatment in PD patients and encourage an early DBS approach, before severe levodopa-induced sequelae may irreparably compromise the patients' QoL. In the future, more focus should lie on sex-related effects, since female patients seem to profit more than male patients from STN-DBS, in terms of reduced depressive symptoms associated with a reduction of the LEDD and amelioration of QoL. These aspects may help to redress the sex imbalance in PD patients treated with DBS, given that women are still strongly under-represented.

Dataset Information

Mapping autonomic, mood and cognitive effects of hypothalamic region deep brain stimulation.

Publications

Mapping autonomic, mood and cognitive effects of hypothalamic region deep brain stimulation.

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