Network-targeted transcranial direct current stimulation of the hypothalamus appetite-control network: a feasibility study.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
18 May 2024
Historique:
received: 31 10 2023
accepted: 10 05 2024
medline: 19 5 2024
pubmed: 19 5 2024
entrez: 18 5 2024
Statut: epublish

Résumé

The hypothalamus is the key regulator for energy homeostasis and is functionally connected to striatal and cortical regions vital for the inhibitory control of appetite. Hence, the ability to non-invasively modulate the hypothalamus network could open new ways for the treatment of metabolic diseases. Here, we tested a novel method for network-targeted transcranial direct current stimulation (net-tDCS) to influence the excitability of brain regions involved in the control of appetite. Based on the resting-state functional connectivity map of the hypothalamus, a 12-channel net-tDCS protocol was generated (Neuroelectrics Starstim system), which included anodal, cathodal and sham stimulation. Ten participants with overweight or obesity were enrolled in a sham-controlled, crossover study. During stimulation or sham control, participants completed a stop-signal task to measure inhibitory control. Overall, stimulation was well tolerated. Anodal net-tDCS resulted in faster stop signal reaction time (SSRT) compared to sham (p = 0.039) and cathodal net-tDCS (p = 0.042). Baseline functional connectivity of the target network correlated with SSRT after anodal compared to sham stimulation (p = 0.016). These preliminary data indicate that modulating hypothalamus functional network connectivity via net-tDCS may result in improved inhibitory control. Further studies need to evaluate the effects on eating behavior and metabolism.

Identifiants

pubmed: 38762574
doi: 10.1038/s41598-024-61852-3
pii: 10.1038/s41598-024-61852-3
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

11341

Subventions

Organisme : DZD e.V.
ID : 01GI0925
Organisme : DZD e.V.
ID : 01GI0925
Organisme : DZD e.V.
ID : 01GI0925
Organisme : DZD e.V.
ID : 01GI0925
Organisme : DZD e.V.
ID : 01GI0925
Organisme : DZD e.V.
ID : 01GI0925
Organisme : DZD e.V.
ID : 01GI0925
Organisme : DZD e.V.
ID : 01GI0925

Informations de copyright

© 2024. The Author(s).

Références

Nitsche, M. A. & Paulus, W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J. Physiol. (Lond ) 527(Pt 3), 633–639 (2000).
pubmed: 10990547 doi: 10.1111/j.1469-7793.2000.t01-1-00633.x
Sreeraj, V. S., Arumugham, S. S. & Venkatasubramanian, G. Clinical practice guidelines for the use of transcranial direct current stimulation in psychiatry. Indian J. Psychiatry 65, 289–296 (2023).
pubmed: 37063621 pmcid: 10096202 doi: 10.4103/indianjpsychiatry.indianjpsychiatry_496_22
Moreno-Duarte, I. et al. Transcranial Electrical Stimulation. In The stimulated brain 35–59 (Elsevier, 2014).
doi: 10.1016/B978-0-12-404704-4.00002-8
Purpura, D. P. & McMurtry, J. G. INTRACELLULAR ACTIVITIES AND EVOKED POTENTIAL CHANGES DURING POLARIZATION OF MOTOR CORTEX. J. Neurophysiol. 28, 166–185 (1965).
pubmed: 14244793 doi: 10.1152/jn.1965.28.1.166
Fertonani, A. & Miniussi, C. Transcranial electrical stimulation: what we know and do not know about mechanisms. Neuroscientist 23, 109–123 (2017).
pubmed: 26873962 doi: 10.1177/1073858416631966
Agboada, D. et al. Expanding the parameter space of anodal transcranial direct current stimulation of the primary motor cortex. Sci. Rep. 9, 18185 (2019).
pubmed: 31796827 pmcid: 6890804 doi: 10.1038/s41598-019-54621-0
Wen, Y.-R. et al. Is transcranial direct current stimulation beneficial for treating pain, depression, and anxiety symptoms in patients with chronic pain? A systematic review and meta-analysis. Front. Mol. Neurosci. 15, 1056966 (2022).
pubmed: 36533133 pmcid: 9752114 doi: 10.3389/fnmol.2022.1056966
Sudbrack-Oliveira, P. et al. Transcranial direct current stimulation (tDCS) in the management of epilepsy: A systematic review. Seizure 86, 85–95 (2021).
pubmed: 33582584 doi: 10.1016/j.seizure.2021.01.020
Giel, K. E. et al. Inhibitory control training enhanced by transcranial direct current stimulation to reduce binge eating episodes: findings from the randomized phase II ACCElect trial. Psychother. Psychosom. 92, 101–112 (2023).
pubmed: 36889293 doi: 10.1159/000529117
Pergher, V. et al. The benefits of simultaneous tDCS and working memory training on transfer outcomes: A systematic review and meta-analysis. Brain Stimul. 15, 1541–1551 (2022).
pubmed: 36460294 doi: 10.1016/j.brs.2022.11.008
Weller, S., Nitsche, M. A. & Plewnia, C. Enhancing cognitive control training with transcranial direct current stimulation: A systematic parameter study. Brain Stimul. 13, 1358–1369 (2020).
pubmed: 32687899 doi: 10.1016/j.brs.2020.07.006
Fregni, F. et al. Evidence-based guidelines and secondary meta-analysis for the use of transcranial direct current stimulation in neurological and psychiatric disorders. Int. J. Neuropsychopharmacol. 24, 256–313 (2021).
pubmed: 32710772 doi: 10.1093/ijnp/pyaa051
Nitsche, M. A. et al. Transcranial direct current stimulation: State of the art 2008. Brain Stimul. 1, 206–223 (2008).
pubmed: 20633386 doi: 10.1016/j.brs.2008.06.004
Dmochowski, J. P. et al. Optimized multi-electrode stimulation increases focality and intensity at target. J. Neural Eng. 8, 46011 (2011).
doi: 10.1088/1741-2560/8/4/046011
van den Heuvel, M. P. & Hulshoff Pol, H. E. Exploring the brain network: A review on resting-state fMRI functional connectivity. Eur. Neuropsychopharmacol. 20, 519–534 (2010).
pubmed: 20471808 doi: 10.1016/j.euroneuro.2010.03.008
Fischer, D. B. et al. Multifocal tDCS targeting the resting state motor network increases cortical excitability beyond traditional tDCS targeting unilateral motor cortex. Neuroimage 157, 34–44 (2017).
pubmed: 28572060 doi: 10.1016/j.neuroimage.2017.05.060
Mencarelli, L. et al. Impact of network-targeted multichannel transcranial direct current stimulation on intrinsic and network-to-network functional connectivity. J. Neurosci. Res. 98, 1843–1856 (2020).
pubmed: 32686203 pmcid: 9094635 doi: 10.1002/jnr.24690
Ruffini, G. et al. Targeting brain networks with multichannel transcranial current stimulation (tCS). Curr. Opin. Biomed. Eng. 8, 70–77 (2018).
doi: 10.1016/j.cobme.2018.11.001
de Klerk, M. T., Smeets, P. A. M. & La Fleur, S. E. Inhibitory control as a potential treatment target for obesity. Nutr. Neurosci. 26, 429–444 (2023).
pubmed: 35343884 doi: 10.1080/1028415X.2022.2053406
Bartholdy, S. et al. A systematic review of the relationship between eating, weight and inhibitory control using the stop signal task. Neurosci. Biobehav. Rev. 64, 35–62 (2016).
pubmed: 26900651 doi: 10.1016/j.neubiorev.2016.02.010
Lavagnino, L. et al. Inhibitory control in obesity and binge eating disorder: A systematic review and meta-analysis of neurocognitive and neuroimaging studies. Neurosci. Biobehav. Rev. 68, 714–726 (2016).
pubmed: 27381956 doi: 10.1016/j.neubiorev.2016.06.041
Angius, L. et al. Transcranial direct current stimulation over the left dorsolateral prefrontal cortex improves inhibitory control and endurance performance in healthy individuals. Neuroscience 419, 34–45 (2019).
pubmed: 31493549 doi: 10.1016/j.neuroscience.2019.08.052
Ester, T. & Kullmann, S. Neurobiological regulation of eating behavior: Evidence based on non-invasive brain stimulation. Rev. Endocr. Metab. Disord. 23(4), 753–772 (2021).
pubmed: 34862944 pmcid: 9307556 doi: 10.1007/s11154-021-09697-3
Schroeder, P. A. et al. Meta-analysis of the effects of transcranial direct current stimulation on inhibitory control. Brain Stimul. 13, 1159–1167 (2020).
pubmed: 32442624 doi: 10.1016/j.brs.2020.05.006
Sheffield, J. M. & Barch, D. M. Cognition and resting-state functional connectivity in schizophrenia. Neurosci. Biobehav. Rev. 61, 108–120 (2016).
pubmed: 26698018 doi: 10.1016/j.neubiorev.2015.12.007
Kohl, S. H. et al. Real-time fMRI neurofeedback training to improve eating behavior by self-regulation of the dorsolateral prefrontal cortex: A randomized controlled trial in overweight and obese subjects. Neuroimage 191, 596–609 (2019).
pubmed: 30798010 doi: 10.1016/j.neuroimage.2019.02.033
Hare, T. A., Camerer, C. F. & Rangel, A. Self-control in decision-making involves modulation of the vmPFC valuation system. Science 324, 646–648 (2009).
pubmed: 19407204 doi: 10.1126/science.1168450
Kullmann, S. & Veit, R. Resting-state functional connectivity of the human hypothalamus. Handb. Clin. Neurol. 179, 113–124 (2021).
pubmed: 34225957 doi: 10.1016/B978-0-12-819975-6.00005-4
Kullmann, S. et al. Resting-state functional connectivity of the human hypothalamus. Hum. Brain Mapp. 35, 6088–6096 (2014).
pubmed: 25131690 pmcid: 6869436 doi: 10.1002/hbm.22607
Kullmann, S. et al. The effect of hunger state on hypothalamic functional connectivity in response to food cues. Hum. Brain Mapp. 44, 418–428 (2023).
pubmed: 36056618 doi: 10.1002/hbm.26059
Menon, V. & D’Esposito, M. The role of PFC networks in cognitive control and executive function. Neuropsychopharmacology 47, 90–103 (2022).
pubmed: 34408276 doi: 10.1038/s41386-021-01152-w
Li, G. et al. Brain functional and structural magnetic resonance imaging of obesity and weight loss interventions. Mol. Psychiatry 28, 1466–1479 (2023).
pubmed: 36918706 pmcid: 10208984 doi: 10.1038/s41380-023-02025-y
Kullmann, S. et al. Central nervous pathways of insulin action in the control of metabolism and food intake. Lancet Diabetes Endocrinol. 8, 524–534 (2020).
pubmed: 32445739 doi: 10.1016/S2213-8587(20)30113-3
Poreisz, C. et al. Safety aspects of transcranial direct current stimulation concerning healthy subjects and patients. Brain Res. Bull. 72, 208–214 (2007).
pubmed: 17452283 doi: 10.1016/j.brainresbull.2007.01.004
Cambridge Neuropsychological Test Automated Battery. Stop Signal Task (SST). The Stop Signal Task is a unique version of a classic approach to measuring response inhibition (impulse control). https://cambridgecognition.com/stop-signal-task-sst/ (31 July 2023, date last Accessed).
Hardung, S., Jäckel, Z. & Diester, I. Prefrontal contributions to action control in rodents. Int. Rev. Neurobiol. 158, 373–393 (2021).
pubmed: 33785152 doi: 10.1016/bs.irn.2020.11.010
Logan, G. D., Schachar, R. J. & Tannock, R. Impulsivity and inhibitory control. Psychol. Sci. 8, 60–64 (1997).
doi: 10.1111/j.1467-9280.1997.tb00545.x
Logan, G. D. et al. On the ability to inhibit thought and action: General and special theories of an act of control. Psychol. Rev. 121, 66–95 (2014).
pubmed: 24490789 doi: 10.1037/a0035230
Ruffini, G. et al. Optimization of multifocal transcranial current stimulation for weighted cortical pattern targeting from realistic modeling of electric fields. Neuroimage 89, 216–225 (2013).
pubmed: 24345389 doi: 10.1016/j.neuroimage.2013.12.002
Miranda, P. C. et al. The electric field in the cortex during transcranial current stimulation. Neuroimage 70, 48–58 (2013).
pubmed: 23274187 doi: 10.1016/j.neuroimage.2012.12.034
Yan, C.-G. et al. DPABI: Data processing & analysis for (resting-state) brain imaging. Neuroinformatics 14, 339–351 (2016).
pubmed: 27075850 doi: 10.1007/s12021-016-9299-4
Song, X.-W. et al. REST: A toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One 6, e25031 (2011).
pubmed: 21949842 pmcid: 3176805 doi: 10.1371/journal.pone.0025031
El Jamal, C. et al. Tolerability and blinding of high-definition transcranial direct current stimulation among older adults at intensities of up to 4 mA per electrode. Brain Stimul. 16, 1328–1335 (2023).
pubmed: 37660936 doi: 10.1016/j.brs.2023.08.025
Reckow, J. et al. Tolerability and blinding of 4 × 1 high-definition transcranial direct current stimulation (HD-tDCS) at two and three milliamps. Brain Stimul. 11, 991–997 (2018).
pubmed: 29784589 pmcid: 6512313 doi: 10.1016/j.brs.2018.04.022
DelParigi, A. et al. Successful dieters have increased neural activity in cortical areas involved in the control of behavior. Int. J. Obes. (Lond) 31, 440–448 (2007).
pubmed: 16819526 doi: 10.1038/sj.ijo.0803431
Chen, F. et al. Increased BOLD signals in dlPFC Is associated with stronger self-control in food-related decision-making. Front. Psychiatry 9, 689 (2018).
pubmed: 30618869 pmcid: 6306453 doi: 10.3389/fpsyt.2018.00689
Max, S. M. et al. Mind the food: behavioural characteristics and imaging signatures of the specific handling of food objects. Brain Struct. Funct. 226, 1169–1183 (2021).
pubmed: 33590302 pmcid: 8036193 doi: 10.1007/s00429-021-02232-9
Wiegand, A. et al. Improvement of cognitive control and stabilization of affect by prefrontal transcranial direct current stimulation (tDCS). Sci. Rep. 9, 6797 (2019).
pubmed: 31043662 pmcid: 6494905 doi: 10.1038/s41598-019-43234-2
Sandrini, M. et al. Transcranial direct current stimulation facilitates response inhibition through dynamic modulation of the fronto-basal ganglia network. Brain Stimul. 13, 96–104 (2020).
pubmed: 31422052 doi: 10.1016/j.brs.2019.08.004
Splittgerber, M. et al. Individual baseline performance and electrode montage impact on the effects of anodal tDCS over the left dorsolateral prefrontal cortex. Front. Hum. Neurosci. 14, 349 (2020).
pubmed: 33100989 pmcid: 7506510 doi: 10.3389/fnhum.2020.00349
Gregoret, L., Zamorano, A. M. & Graven-Nielsen, T. Multifocal tDCS targeting the motor network modulates event-related cortical responses during prolonged pain. J. Pain 24, 226–236 (2023).
pubmed: 36162791 doi: 10.1016/j.jpain.2022.09.010
Guo, Z. et al. Multitarget high-definition transcranial direct current stimulation improves response inhibition more than single-target high-definition transcranial direct current stimulation in healthy participants. Front. Neurosci. 16, 905247 (2022).
pubmed: 35968393 pmcid: 9372262 doi: 10.3389/fnins.2022.905247
Fox, M. D. et al. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. U S A 102, 9673–9678 (2005).
pubmed: 15976020 pmcid: 1157105 doi: 10.1073/pnas.0504136102
Cerit, H. et al. Resting-state brain connectivity predicts weight loss and cognitive control of eating behavior after vertical sleeve gastrectomy. Obesity (Silver Spring) 27, 1846–1855 (2019).
pubmed: 31689011 doi: 10.1002/oby.22607
Yu, J. et al. Brain stimulation improves cognitive control by modulating medial-frontal activity and preSMA-vmPFC functional connectivity. Hum. Brain Mapp. 36, 4004–4015 (2015).
pubmed: 26248582 pmcid: 6869595 doi: 10.1002/hbm.22893
Weygandt, M. et al. The role of neural impulse control mechanisms for dietary success in obesity. Neuroimage 83, 669–678 (2013).
pubmed: 23867558 doi: 10.1016/j.neuroimage.2013.07.028
Spetter, M. S. et al. Volitional regulation of brain responses to food stimuli in overweight and obese subjects: A real-time fMRI feedback study. Appetite 112, 188–195 (2017).
pubmed: 28131758 doi: 10.1016/j.appet.2017.01.032
Corriveau, A. et al. Functional connectome stability and optimality are markers of cognitive performance. Cereb. Cortex 33, 5025–5041 (2023).
pubmed: 36408606 doi: 10.1093/cercor/bhac396
Lin, Q. et al. Resting-State Functional Connectivity Predicts Cognitive Impairment Related to Alzheimer’s Disease. Front. Aging Neurosci. 10, 94 (2018).
pubmed: 29706883 pmcid: 5908906 doi: 10.3389/fnagi.2018.00094
Braun, U., Muldoon, S. F. & Bassett, D. S. On Human Brain Networks in Health and Disease. In Encyclopedia of life sciences 1–9 (Wiley, 2005).
Le, T. M. et al. The interrelationship of body mass index with gray matter volume and resting-state functional connectivity of the hypothalamus. Int. J. Obes. (Lond) 44, 1097–1107 (2020).
pubmed: 31796869 doi: 10.1038/s41366-019-0496-8
Kullmann, S. et al. Intranasal insulin enhances brain functional connectivity mediating the relationship between adiposity and subjective feeling of hunger. Sci. Rep. 7, 1627 (2017).
pubmed: 28487570 pmcid: 5431641 doi: 10.1038/s41598-017-01907-w
Kullmann, S. et al. Central insulin modulates dopamine signaling in the human striatum. J. Clin. Endocrinol. Metab. 106, 2949–2961 (2021).
pubmed: 34131733 doi: 10.1210/clinem/dgab410

Auteurs

Theresa Ester-Nacke (T)

Institute for Diabetes Research and Metabolic Diseases (IDM) of the Helmholtz Center Munich at the University of Tübingen, Tübingen, Germany. Theresa.ester@med.uni-tuebingen.de.
Department of Internal Medicine, Division of Endocrinology, Diabetology and Nephrology, Eberhard Karls University Tübingen, Tübingen, Germany. Theresa.ester@med.uni-tuebingen.de.
German Center of Diabetes Research (DZD), Tübingen, Germany. Theresa.ester@med.uni-tuebingen.de.

Katharina Berti (K)

Institute for Diabetes Research and Metabolic Diseases (IDM) of the Helmholtz Center Munich at the University of Tübingen, Tübingen, Germany.
Department of Internal Medicine, Division of Endocrinology, Diabetology and Nephrology, Eberhard Karls University Tübingen, Tübingen, Germany.
German Center of Diabetes Research (DZD), Tübingen, Germany.

Ralf Veit (R)

Institute for Diabetes Research and Metabolic Diseases (IDM) of the Helmholtz Center Munich at the University of Tübingen, Tübingen, Germany.
Department of Internal Medicine, Division of Endocrinology, Diabetology and Nephrology, Eberhard Karls University Tübingen, Tübingen, Germany.
German Center of Diabetes Research (DZD), Tübingen, Germany.

Corinna Dannecker (C)

Institute for Diabetes Research and Metabolic Diseases (IDM) of the Helmholtz Center Munich at the University of Tübingen, Tübingen, Germany.
Department of Internal Medicine, Division of Endocrinology, Diabetology and Nephrology, Eberhard Karls University Tübingen, Tübingen, Germany.
German Center of Diabetes Research (DZD), Tübingen, Germany.

Ricardo Salvador (R)

Neuroelectrics Barcelona, Barcelona, Spain.

Giulio Ruffini (G)

Neuroelectrics Barcelona, Barcelona, Spain.

Martin Heni (M)

Institute for Diabetes Research and Metabolic Diseases (IDM) of the Helmholtz Center Munich at the University of Tübingen, Tübingen, Germany.
Department of Internal Medicine, Division of Endocrinology, Diabetology and Nephrology, Eberhard Karls University Tübingen, Tübingen, Germany.
German Center of Diabetes Research (DZD), Tübingen, Germany.
Department for Diagnostic Laboratory Medicine, Institute for Clinical Chemistry and Pathobiochemistry, Eberhard Karls University Tübingen, Tübingen, Germany.
Division of Endocrinology and Diabetology, Department of Internal Medicine 1, University Hospital Ulm, Ulm, Germany.

Andreas L Birkenfeld (AL)

Institute for Diabetes Research and Metabolic Diseases (IDM) of the Helmholtz Center Munich at the University of Tübingen, Tübingen, Germany.
Department of Internal Medicine, Division of Endocrinology, Diabetology and Nephrology, Eberhard Karls University Tübingen, Tübingen, Germany.
German Center of Diabetes Research (DZD), Tübingen, Germany.

Christian Plewnia (C)

Department of Psychiatry and Psychotherapy, German Center for Mental Health (DZPG), Neurophysiology and Interventional Neuropsychiatry, University Hospital Tübingen, Tübingen, Germany.

Hubert Preissl (H)

Institute for Diabetes Research and Metabolic Diseases (IDM) of the Helmholtz Center Munich at the University of Tübingen, Tübingen, Germany.
Department of Internal Medicine, Division of Endocrinology, Diabetology and Nephrology, Eberhard Karls University Tübingen, Tübingen, Germany.
German Center of Diabetes Research (DZD), Tübingen, Germany.

Stephanie Kullmann (S)

Institute for Diabetes Research and Metabolic Diseases (IDM) of the Helmholtz Center Munich at the University of Tübingen, Tübingen, Germany.
Department of Internal Medicine, Division of Endocrinology, Diabetology and Nephrology, Eberhard Karls University Tübingen, Tübingen, Germany.
German Center of Diabetes Research (DZD), Tübingen, Germany.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH