Deep TMS of the insula using the H-coil modulates dopamine release: a crossover [11C] PHNO-PET pilot trial in healthy humans

Malik, Saima; Jacobs, Mark; Cho, Sang-Soo; Boileau, Isabelle; Blumberger, Daniel; Heilig, Markus; Wilson, Alan; Daskalakis, Zafiris J.; Strafella, Antonio P.; Zangen, Abraham; Le Foll, Bernard

doi:10.1007/s11682-017-9800-1

Original Research
Published: 23 November 2017

Deep TMS of the insula using the H-coil modulates dopamine release: a crossover [¹¹C] PHNO-PET pilot trial in healthy humans

Saima Malik¹,
Mark Jacobs^2,3,
Sang-Soo Cho^2,3,
Isabelle Boileau²,
Daniel Blumberger^4,5,6,
Markus Heilig⁷,
Alan Wilson²,
Zafiris J. Daskalakis^4,5,6,
Antonio P. Strafella^2,3,8,
Abraham Zangen⁹ &
Bernard Le Foll^1,4,6,10

Brain Imaging and Behavior volume 12, pages 1306–1317 (2018)Cite this article

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Abstract

Modulating the function of the insular cortex could be a novel therapeutic strategy to treat addiction to a variety of drugs of abuse as this region has been implicated in mediating drug reward and addictive processes. The recent advent of the H-coil has permitted the targeting of deeper brain structures which was not previously feasible. The goal of this study was to bilaterally target the insular region using the H-coil with repetitive Transcranial Magnetic Stimulation (rTMS) and subsequently measure changes in dopamine levels using Positron Emission Tomography (PET) with [11C]-(+)-propyl-hexahydro-naphtho-oxazin (PHNO). This was a within-subject, crossover, blinded and sham-controlled pilot study. Eight healthy, right-handed subjects, aged 19–45, participated in the investigation. All subjects underwent 3 PHNO-PET scans preceded by rTMS (sham, 1 Hz or 10 Hz), on 3 separate days. Low frequency rTMS (1 Hz), targeting the insular cortex, significantly decreased dopamine levels in the substantia nigra, sensorimotor striatum and associative striatum. Replicating this study in tobacco smokers or alcoholics would be a logical follow-up to assess whether H-coil stimulation of the bilateral insula can be employed as a treatment option for addiction. Trial registration: NCT02212405

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Abbreviations

RTMS:: Repeated Transcranial Magnetic Stimulation
PET:: Positron Emission Tomography
PHNO:: [11C]-(+)-propyl-hexahydro-naphtho-oxazin
BPND:: [11C]-(+)-PHNO specific binding

References

Amiaz, R., Levy, D., Vainiger, D., Grunhaus, L., & Zangen, A. (2009). Repeated high-frequency transcranial magnetic stimulation over the dorsolateral prefrontal cortex reduces cigarette craving and consumption. Addiction, 104(4), 653–660. https://doi.org/10.1111/j.1360-0443.2008.02448.x.
Article PubMed Google Scholar
Augustine, J. R. (1996). Circuitry and functional aspects of the insular lobe in primates including humans. Brain Research Brain Research Reviews, 22(3), 229–244.
CAS Article Google Scholar
Barrett, S. P., Boileau, I., Okker, J., Pihl, R. O., & Dagher, A. (2004). The hedonic response to cigarette smoking is proportional to dopamine release in the human striatum as measured by positron emission tomography and [11C]raclopride. Synapse, 54(2), 65–71. https://doi.org/10.1002/syn.20066.
CAS Article PubMed Google Scholar
Berridge, K. C., & Robinson, T. E. (1998). What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Research Brain Research Reviews, 28(3), 309–369.
CAS Article Google Scholar
Bestmann, S., Baudewig, J., Siebner, H. R., Rothwell, J. C., & Frahm, J. (2005). BOLD MRI responses to repetitive TMS over human dorsal premotor cortex. Neuroimage, 28(1), 22–29. https://doi.org/10.1016/j.neuroimage.2005.05.027.
Article PubMed Google Scholar
Boileau, I., Assaad, J. M., Pihl, R. O., Benkelfat, C., Leyton, M., Diksic, M., … Dagher, A. (2003). Alcohol promotes dopamine release in the human nucleus accumbens. Synapse, 49(4), 226–231. https://doi.org/10.1002/syn.10226.
CAS Article PubMed Google Scholar
Boileau, I., Payer, D., Houle, S., Behzadi, A., Rusjan, P. M., Tong, J., … Kish, S. J. (2012). Higher binding of the dopamine D3 receptor-preferring ligand [11C]-(+)-propyl-hexahydro-naphtho-oxazin in methamphetamine polydrug users: a positron emission tomography study. Journal of Neuroscience, 32(4), 1353–1359. https://doi.org/10.1523/JNEUROSCI.4371-11.2012.
CAS Article PubMed Google Scholar
Boileau, I., Payer, D., Rusjan, P. M., Houle, S., Tong, J., McCluskey, T., … Kish, S. J. (2016). Heightened dopaminergic response to amphetamine at the D3 dopamine receptor in methamphetamine users. Neuropsychopharmacology, 41(13), 2994–3002. https://doi.org/10.1038/npp.2016.108.
CAS Article PubMed PubMed Central Google Scholar
Bossong, M. G., van Berckel, B. N., Boellaard, R., Zuurman, L., Schuit, R. C., Windhorst, A. D., … Kahn, R. S. (2009). Delta 9-tetrahydrocannabinol induces dopamine release in the human striatum. Neuropsychopharmacology, 34(3), 759–766. https://doi.org/10.1038/npp.2008.138.
CAS Article PubMed Google Scholar
Camprodon, J. A., Martinez-Raga, J., Alonso-Alonso, M., Shih, M. C., & Pascual-Leone, A. (2007). One session of high frequency repetitive transcranial magnetic stimulation (rTMS) to the right prefrontal cortex transiently reduces cocaine craving. Drug and Alcohol Dependence, 86(1), 91–94. https://doi.org/10.1016/j.drugalcdep.2006.06.002.
Article PubMed Google Scholar
Cardenas, L., Houle, S., Kapur, S., & Busto, U. E. (2004). Oral D-amphetamine causes prolonged displacement of [11C]raclopride as measured by PET. Synapse, 51(1), 27–31. https://doi.org/10.1002/syn.10282.
CAS Article PubMed Google Scholar
Carson, R. E., Breier, A., de Bartolomeis, A., Saunders, R. C., Su, T. P., Schmall, B., … Eckelman, W. C. (1997). Quantification of amphetamine-induced changes in [11C]raclopride binding with continuous infusion. Journal of Cerebral Blood Flow Metabolism, 17(4), 437–447. https://doi.org/10.1097/00004647-199704000-00009.
CAS Article PubMed Google Scholar
Cho, S. S., & Strafella, A. P. (2009). rTMS of the left dorsolateral prefrontal cortex modulates dopamine release in the ipsilateral anterior cingulate cortex and orbitofrontal cortex. PLoS One, 4(8), e6725. https://doi.org/10.1371/journal.pone.0006725.
CAS Article PubMed PubMed Central Google Scholar
Contreras, M., Billeke, P., Vicencio, S., Madrid, C., Perdomo, G., Gonzalez, M., & Torrealba, F. (2012). A role for the insular cortex in long-term memory for context-evoked drug craving in rats. Neuropsychopharmacology, 37(9), 2101–2108. https://doi.org/10.1038/npp.2012.59.
CAS Article PubMed PubMed Central Google Scholar
Contreras, M., Ceric, F., & Torrealba, F. (2007). Inactivation of the interoceptive insula disrupts drug craving and malaise induced by lithium. Science, 318(5850), 655–658. https://doi.org/10.1126/science.1145590.
CAS Article PubMed Google Scholar
Daskalakis, Z. J., Levinson, A. J., & Fitzgerald, P. B. (2008). Repetitive transcranial magnetic stimulation for major depressive disorder: a review. Canadian Journal of Psychiatry, 53(9), 555–566.
Article Google Scholar
Daskalakis, Z. J., Moller, B., Christensen, B. K., Fitzgerald, P. B., Gunraj, C., & Chen, R. (2006). The effects of repetitive transcranial magnetic stimulation on cortical inhibition in healthy human subjects. Experimental Brain Reseach, 174(3), 403–412. https://doi.org/10.1007/s00221-006-0472-0.
Article Google Scholar
de Jesus, D. R., Favalli, G. P., Hoppenbrouwers, S. S., Barr, M. S., Chen, R., Fitzgerald, P. B., & Daskalakis, Z. J. (2014). Determining optimal rTMS parameters through changes in cortical inhibition. Clinical Neurophysiology, 125(4), 755–762. https://doi.org/10.1016/j.clinph.2013.09.011.
Article PubMed Google Scholar
Di Chiara, G. (2000). Role of dopamine in the behavioural actions of nicotine related to addiction. European Journal of Pharmacology, 393(1–3), 295–314.
Article Google Scholar
Di Chiara, G. (2002). Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behavioural Brain Research, 137(1–2), 75–114.
Article Google Scholar
Dinur-Klein, L., Dannon, P., Hadar, A., Rosenberg, O., Roth, Y., Kotler, M., & Zangen, A. (2014). Smoking cessation induced by deep repetitive transcranial magnetic stimulation of the prefrontal and insular cortices: a prospective, randomized controlled trial. Biological Psychiatry, 76(9), 742–749. https://doi.org/10.1016/j.biopsych.2014.05.020.
Article PubMed Google Scholar
Droutman, V., Read, S. J., & Bechara, A. (2015). Revisiting the role of the insula in addiction. Trends in Cognitive Sciences, 19(7), 414–420. https://doi.org/10.1016/j.tics.2015.05.005.
Article PubMed PubMed Central Google Scholar
Everitt, B. J., Dickinson, A., & Robbins, T. W. (2001). The neuropsychological basis of addictive behaviour. Brain Research Brain Research Reviews, 36(2–3), 129–138.
CAS Article Google Scholar
Everitt, B. J., Parkinson, J. A., Olmstead, M. C., Arroyo, M., Robledo, P., & Robbins, T. W. (1999). Associative processes in addiction and reward. The role of amygdala-ventral striatal subsystems. Annals of the New York Academy of Sciences, 877, 412–438.
CAS Article Google Scholar
Feil, J., & Zangen, A. (2010). Brain stimulation in the study and treatment of addiction. Neuroscience & Biobehavioral Reviews, 34(4), 559–574. https://doi.org/10.1016/j.neubiorev.2009.11.006.
Article Google Scholar
First, M., Spitzer, R. L., Gibbon, M., & Williams, J. B. (2002). Structured clinical interview for DSM-IV-TR axis I disorders, research version, non-patient edition. (SCID-I/NP). New York: Biometrics Research, New York State Psychiatric Institute.
Google Scholar
Fitzgerald, P. B., Fountain, S., & Daskalakis, Z. J. (2006). A comprehensive review of the effects of rTMS on motor cortical excitability and inhibition. Clinical Neurophysiology, 117(12), 2584–2596. https://doi.org/10.1016/j.clinph.2006.06.712.
Article PubMed Google Scholar
Fitzgerald, P. B., Hoy, K., McQueen, S., Maller, J. J., Herring, S., Segrave, R., … Daskalakis, Z. J. (2009). A randomized trial of rTMS targeted with MRI based neuro-navigation in treatment-resistant depression. Neuropsychopharmacology, 34(5), 1255–1262. https://doi.org/10.1038/npp.2008.233.
Article PubMed Google Scholar
Forget, B., Pushparaj, A., & Le Foll, B. (2010). Granular insular cortex inactivation as a novel therapeutic strategy for nicotine addiction. Biological Psychiatry, 68(3), 265–271. https://doi.org/10.1016/j.biopsych.2010.01.029.
CAS Article PubMed Google Scholar
Garavan, H. (2010). Insula and drug cravings. Brain Structure Function, 214(5–6), 593–601. https://doi.org/10.1007/s00429-010-0259-8.
Article PubMed Google Scholar
Gasquoine, P. G. (2014). Contributions of the insula to cognition and emotion. Neuropsychology Review, 24(2), 77–87. https://doi.org/10.1007/s11065-014-9246-9.
Article PubMed Google Scholar
Gersner, R., Kravetz, E., Feil, J., Pell, G., & Zangen, A. (2011). Long-term effects of repetitive transcranial magnetic stimulation on markers for neuroplasticity: differential outcomes in anesthetized and awake animals. Journal of Neuroscience, 31(20), 7521–7526. https://doi.org/10.1523/JNEUROSCI.6751-10.2011.
CAS Article PubMed Google Scholar
Ginovart, N., Galineau, L., Willeit, M., Mizrahi, R., Bloomfield, P. M., Seeman, P., … Wilson, A. A. (2006). Binding characteristics and sensitivity to endogenous dopamine of [11C]-(+)-PHNO, a new agonist radiotracer for imaging the high-affinity state of D2 receptors in vivo using positron emission tomography. Journal of Neurochemistry, 97(4), 1089–1103. https://doi.org/10.1111/j.1471-4159.2006.03840.x.
CAS Article PubMed Google Scholar
Ginovart, N., Willeit, M., Rusjan, P., Graff, A., Bloomfield, P. M., Houle, S., … Wilson, A. A. (2007). Positron emission tomography quantification of [11C]-(+)-PHNO binding in the human brain. Journal of Cerebral Blood Flow & Metabolism, 27(4), 857–871. https://doi.org/10.1038/sj.jcbfm.9600411.
CAS Article Google Scholar
Ginovart, N., Wilson, A. A., Houle, S., & Kapur, S. (2004). Amphetamine pretreatment induces a change in both D2-Receptor density and apparent affinity: a [11C]raclopride positron emission tomography study in cats. Biological Psychiatry, 55(12), 1188–1194. https://doi.org/10.1016/j.biopsych.2004.02.019.
CAS Article PubMed Google Scholar
Gorelick, D. A., Zangen, A., & George, M. S. (2014). Transcranial magnetic stimulation in the treatment of substance addiction. Annals of the New York Academy of Sciences, 1327, 79–93. https://doi.org/10.1111/nyas.12479.
CAS Article PubMed PubMed Central Google Scholar
Graff-Guerrero, A., Willeit, M., Ginovart, N., Mamo, D., Mizrahi, R., Rusjan, P., … Kapur, S. (2008). Brain region binding of the D2/3 agonist [11C]-(+)-PHNO and the D2/3 antagonist [11C]raclopride in healthy humans. Human Brain Mapping, 29(4), 400–410. https://doi.org/10.1002/hbm.20392.
Article PubMed Google Scholar
Grall-Bronnec, M., & Sauvaget, A. (2014). The use of repetitive transcranial magnetic stimulation for modulating craving and addictive behaviours: a critical literature review of efficacy, technical and methodological considerations. Neuroscience Biobehavioral Reviews, 47, 592–613. https://doi.org/10.1016/j.neubiorev.2014.10.013.
CAS Article PubMed Google Scholar
Hanlon, C. A., Jones, E. M., Li, X., Hartwell, K. J., Brady, K. T., & George, M. S. (2012). Individual variability in the locus of prefrontal craving for nicotine: implications for brain stimulation studies and treatments. Drug and Alcohol Dependence, 125(3), 239–243. https://doi.org/10.1016/j.drugalcdep.2012.02.019.
CAS Article PubMed PubMed Central Google Scholar
Hayashi, T., Ko, J. H., Strafella, A. P., & Dagher, A. (2013). Dorsolateral prefrontal and orbitofrontal cortex interactions during self-control of cigarette craving. Proceedings of the National Academy of Sciences of the United States of America, 110(11), 4422–4427. https://doi.org/10.1073/pnas.1212185110.
Article PubMed PubMed Central Google Scholar
Hoogendam, J. M., Ramakers, G. M., & Di Lazzaro, V. (2010). Physiology of repetitive transcranial magnetic stimulation of the human brain. Brain Stimulation, 3(2), 95–118. https://doi.org/10.1016/j.brs.2009.10.005.
Article PubMed Google Scholar
Jansen, J. M., Daams, J. G., Koeter, M. W., Veltman, D. J., van den Brink, W., & Goudriaan, A. E. (2013). Effects of non-invasive neurostimulation on craving: a meta-analysis. Neuroscience Biobehavioral Reviews, 37(10 Pt 2), 2472–2480. https://doi.org/10.1016/j.neubiorev.2013.07.009.
Article PubMed Google Scholar
Karreman, M., & Moghaddam, B. (1996). The prefrontal cortex regulates the basal release of dopamine in the limbic striatum: an effect mediated by ventral tegmental area. Journal of Neurochemistry, 66(2), 589–598.
CAS Article Google Scholar
Keck, M. E., Sillaber, I., Ebner, K., Welt, T., Toschi, N., Kaehler, S. T., … Engelmann, M. (2000). Acute transcranial magnetic stimulation of frontal brain regions selectively modulates the release of vasopressin, biogenic amines and amino acids in the rat brain. European Journal Neuroscience, 12(10), 3713–3720.
CAS Article Google Scholar
Keck, M. E., Welt, T., Muller, M. B., Erhardt, A., Ohl, F., Toschi, N., … Sillaber, I. (2002). Repetitive transcranial magnetic stimulation increases the release of dopamine in the mesolimbic and mesostriatal system. Neuropharmacology, 43(1), 101–109.
CAS Article Google Scholar
Ko, J. H., Tang, C. C., & Eidelberg, D. (2013). Brain stimulation and functional imaging with fMRI and PET. Handbok of Clinical Neurology, 116, 77–95. https://doi.org/10.1016/B978-0-444-53497-2.00008-5.
Article Google Scholar
Lammertsma, A. A., & Hume, S. P. (1996). Simplified reference tissue model for PET receptor studies. Neuroimage, 4(3 Pt 1), 153–158. https://doi.org/10.1006/nimg.1996.0066.
CAS Article PubMed Google Scholar
Lee, L., Siebner, H. R., Rowe, J. B., Rizzo, V., Rothwell, J. C., Frackowiak, R. S., & Friston, K. J. (2003). Acute remapping within the motor system induced by low-frequency repetitive transcranial magnetic stimulation. Journal of Neuroscience, 23(12), 5308–5318.
CAS Article Google Scholar
Martinez, D., Slifstein, M., Broft, A., Mawlawi, O., Hwang, D. R., Huang, Y., … Laruelle, M. (2003). Imaging human mesolimbic dopamine transmission with positron emission tomography. Part II: amphetamine-induced dopamine release in the functional subdivisions of the striatum. Journal of Cerebral Blood Flow & Metabolism, 23(3), 285–300.
CAS Article Google Scholar
Mylius, V., Ayache, S. S., Ahdab, R., Farhat, W. H., Zouari, H. G., Belke, M., … Lefaucheur, J. P. (2013). Definition of DLPFC and M1 according to anatomical landmarks for navigated brain stimulation: inter-rater reliability, accuracy, and influence of gender and age. Neuroimage, 78, 224–232. https://doi.org/10.1016/j.neuroimage.2013.03.061.
CAS Article PubMed Google Scholar
Naqvi, N. H., & Bechara, A. (2009). The hidden island of addiction: the insula. Trends Neuroscience, 32(1), 56–67. https://doi.org/10.1016/j.tins.2008.09.009.
CAS Article Google Scholar
Naqvi, N. H., & Bechara, A. (2010). The insula and drug addiction: an interoceptive view of pleasure, urges, and decision-making. Brain Structure and Function, 214(5–6), 435–450. https://doi.org/10.1007/s00429-010-0268-7.
Article PubMed Google Scholar
Naqvi, N. H., Gaznick, N., Tranel, D., & Bechara, A. (2014). The insula: a critical neural substrate for craving and drug seeking under conflict and risk. Annals of the New York Academy of Sciences, 1316, 53–70. https://doi.org/10.1111/nyas.12415.
Article PubMed PubMed Central Google Scholar
Naqvi, N. H., Rudrauf, D., Damasio, H., & Bechara, A. (2007). Damage to the insula disrupts addiction to cigarette smoking. Science, 315(5811), 531–534. https://doi.org/10.1126/science.1135926.
CAS Article PubMed PubMed Central Google Scholar
Narendran, R., Slifstein, M., Guillin, O., Hwang, Y., Hwang, D. R., Scher, E., … Laruelle, M. (2006). Dopamine (D2/3) receptor agonist positron emission tomography radiotracer [11C]-(+)-PHNO is a D3 receptor preferring agonist in vivo. Synapse, 60(7), 485–495. https://doi.org/10.1002/syn.20325.
CAS Article PubMed Google Scholar
Noda, Y., Silverstein, W. K., Barr, M. S., Vila-Rodriguez, F., Downar, J., Rajji, T. K., Blumberger, D. M. (2015). Neurobiological mechanisms of repetitive transcranial magnetic stimulation of the dorsolateral prefrontal cortex in depression: a systematic review. Psychological Medicine, 45(16), 3411–3432. https://doi.org/10.1017/S0033291715001609.
CAS Article PubMed Google Scholar
O’Shea, J., Johansen-Berg, H., Trief, D., Gobel, S., & Rushworth, M. F. (2007). Functionally specific reorganization in human premotor cortex. Neuron, 54(3), 479–490. https://doi.org/10.1016/j.neuron.2007.04.021.
CAS Article PubMed Google Scholar
Parvaz, M. A., Alia-Klein, N., Woicik, P. A., Volkow, N. D., & Goldstein, R. Z. (2011). Neuroimaging for drug addiction and related behaviors. Reviews Neuroscience, 22(6), 609–624. https://doi.org/10.1515/RNS.2011.055.
CAS Article Google Scholar
Pascual-Leone, A., Valls-Sole, J., Wassermann, E. M., & Hallett, M. (1994). Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain, 117(Pt 4), 847–858.
Article Google Scholar
Peleman, K., Van Schuerbeek, P., Luypaert, R., Stadnik, T., De Raedt, R., De Mey, J., … Baeken, C. (2010). Using 3D-MRI to localize the dorsolateral prefrontal cortex in TMS research. World Journal of Biological Psychiatry, 11(2 Pt 2), 425–430. https://doi.org/10.1080/15622970802669564.
Article PubMed Google Scholar
Pell, G. S., Roth, Y., & Zangen, A. (2011). Modulation of cortical excitability induced by repetitive transcranial magnetic stimulation: influence of timing and geometrical parameters and underlying mechanisms. Progress Neurobiology, 93(1), 59–98. https://doi.org/10.1016/j.pneurobio.2010.10.003.
Article Google Scholar
Pogarell, O., Koch, W., Popperl, G., Tatsch, K., Jakob, F., Mulert, C., … Padberg, F. (2007). Acute prefrontal rTMS increases striatal dopamine to a similar degree as D-amphetamine. Psychiatry Research, 156(3), 251–255. https://doi.org/10.1016/j.pscychresns.2007.05.002.
CAS Article PubMed Google Scholar
Pogarell, O., Koch, W., Popperl, G., Tatsch, K., Jakob, F., Zwanzger, P., … Padberg, F. (2006). Striatal dopamine release after prefrontal repetitive transcranial magnetic stimulation in major depression: preliminary results of a dynamic [123I] IBZM SPECT study. Journal of Psychiatric Research, 40(4), 307–314. https://doi.org/10.1016/j.jpsychires.2005.09.001.
Article PubMed Google Scholar
Pushparaj, A., Hamani, C., Yu, W., Shin, D. S., Kang, B., Nobrega, J. N., & Le Foll, B. (2013). Electrical stimulation of the insular region attenuates nicotine-taking and nicotine-seeking behaviors. Neuropsychopharmacology, 38(4), 690–698. https://doi.org/10.1038/npp.2012.235.
CAS Article PubMed Google Scholar
Rabiner, E. A., Slifstein, M., Nobrega, J., Plisson, C., Huiban, M., Raymond, R., … Laruelle, M. A. (2009). In vivo quantification of regional dopamine-D3 receptor binding potential of (+)-PHNO: Studies in non-human primates and transgenic mice. Synapse, 63(9), 782–793. https://doi.org/10.1002/syn.20658.
CAS Article PubMed Google Scholar
Robbins, T. W., Cador, M., Taylor, J. R., & Everitt, B. J. (1989). Limbic-striatal interactions in reward-related processes. Neuroscience & Biobehavioral Reviews, 13(2–3), 155–162.
CAS Article Google Scholar
Roth, Y., Amir, A., Levkovitz, Y., & Zangen, A. (2007). Three-dimensional distribution of the electric field induced in the brain by transcranial magnetic stimulation using figure-8 and deep H-coils. Journal of Clinical Neurophysiology, 24(1), 31–38. https://doi.org/10.1097/WNP.0b013e31802fa393.
Article PubMed Google Scholar
Roth, Y., Zangen, A., & Hallett, M. (2002). A coil design for transcranial magnetic stimulation of deep brain regions. Journal of Clinical Neurophysiology, 19(4), 361–370.
Article Google Scholar
Rusjan, P., Mamo, D., Ginovart, N., Hussey, D., Vitcu, I., Yasuno, F.,… Kapur, S. (2006). An automated method for the extraction of regional data from PET images. Psychiatry Research, 147(1), 79–89. https://doi.org/10.1016/j.pscychresns.2006.01.011.
Article PubMed Google Scholar
Salamone, J. D. (1992). Complex motor and sensorimotor functions of striatal and accumbens dopamine: involvement in instrumental behavior processes. Psychopharmacology (Berlin), 107(2–3), 160–174.
CAS Article Google Scholar
Salamone, J. D., & Correa, M. (2002). Motivational views of reinforcement: implications for understanding the behavioral functions of nucleus accumbens dopamine. Behavioural Brain Research, 137(1–2), 3–25.
CAS Article Google Scholar
Salamone, J. D., Correa, M., Mingote, S., & Weber, S. M. (2003). Nucleus accumbens dopamine and the regulation of effort in food-seeking behavior: implications for studies of natural motivation, psychiatry, and drug abuse. Journal of Pharmacology Experimental Therapeutics, 305(1), 1–8. https://doi.org/10.1124/jpet.102.035063.
CAS Article PubMed Google Scholar
Schultz, W. (2002). Getting formal with dopamine and reward. Neuron, 36(2), 241–263.
CAS Article Google Scholar
Schultz, W. (2006). Behavioral theories and the neurophysiology of reward. Annual Review of Psychology, 57, 87–115. https://doi.org/10.1146/annurev.psych.56.091103.070229.
Article PubMed Google Scholar
Schultz, W., Dayan, P., & Montague, P. R. (1997). A neural substrate of prediction and reward. Science, 275(5306), 1593–1599.
CAS Article Google Scholar
Scott, D., & Hiroi, N. (2011). Deconstructing craving: dissociable cortical control of cue reactivity in nicotine addiction. Biological Psychiatry, 69(11), 1052–1059. https://doi.org/10.1016/j.biopsych.2011.01.023.
CAS Article PubMed PubMed Central Google Scholar
Shalev, U., Grimm, J. W., & Shaham, Y. (2002). Neurobiology of relapse to heroin and cocaine seeking: a review. Pharmacological Reviews, 54(1), 1–42.
CAS Article Google Scholar
Shotbolt, P., Tziortzi, A. C., Searle, G. E., Colasanti, A., van der Aart, J., Abanades, S., … Rabiner, E. A. (2012). Within-subject comparison of [(11)C]-(+)-PHNO and [(11)C]raclopride sensitivity to acute amphetamine challenge in healthy humans. Journal of Cerebral Blood Flow & Metabolism, 32(1), 127–136. https://doi.org/10.1038/jcbfm.2011.115.
CAS Article Google Scholar
Strafella, A. P., Paus, T., Barrett, J., & Dagher, A. (2001). Repetitive transcranial magnetic stimulation of the human prefrontal cortex induces dopamine release in the caudate nucleus. Journal of Neuroscience, 21(15), RC157.
CAS Article Google Scholar
Strafella, A. P., Paus, T., Fraraccio, M., & Dagher, A. (2003). Striatal dopamine release induced by repetitive transcranial magnetic stimulation of the human motor cortex. Brain, 126(Pt 12), 2609–2615. https://doi.org/10.1093/brain/awg268.
Article PubMed Google Scholar
Trojak, B., Meille, V., Achab, S., Lalanne, L., Poquet, H., Ponavoy, E.,… Chauvet-Gelinier, J. C. (2015). Transcranial magnetic stimulation combined with nicotine replacement therapy for smoking cessation: a randomized controlled trial. Brain Stimulation, 8(6), 1168–1174. https://doi.org/10.1016/j.brs.2015.06.004.
Article PubMed Google Scholar
Tsukada, H., Miyasato, K., Kakiuchi, T., Nishiyama, S., Harada, N., & Domino, E. F. (2002). Comparative effects of methamphetamine and nicotine on the striatal [(11)C]raclopride binding in unanesthetized monkeys. Synapse, 45(4), 207–212. https://doi.org/10.1002/syn.10102.
CAS Article PubMed Google Scholar
Volkow, N. D., & Baler, R. D. (2015). NOW vs LATER brain circuits: implications for obesity and addiction. Trends in Neurosciences, 38(6), 345–352. https://doi.org/10.1016/j.tins.2015.04.002.
CAS Article PubMed Google Scholar
Volkow, N. D., Fowler, J. S., Wang, G. J., Baler, R., & Telang, F. (2009). Imaging dopamine’s role in drug abuse and addiction. Neuropharmacology, 56 Suppl 1, 3–8. https://doi.org/10.1016/j.neuropharm.2008.05.022.
CAS Article PubMed Google Scholar
Willeit, M., Ginovart, N., Graff, A., Rusjan, P., Vitcu, I., Houle, S., … Kapur, S. (2008). First human evidence of d-amphetamine induced displacement of a D2/3 agonist radioligand: a [11C]-(+)-PHNO positron emission tomography study. Neuropsychopharmacology, 33(2), 279–289. https://doi.org/10.1038/sj.npp.1301400.
CAS Article PubMed Google Scholar
Wilson, A. A., McCormick, P., Kapur, S., Willeit, M., Garcia, A., Hussey, D., … Ginovart, N. (2005). Radiosynthesis and evaluation of [11C]-(+)-4-propyl-3,4,4a,5,6,10b-hexahydro-2H-naphtho[1,2-b][1,4]oxazin-9 -ol as a potential radiotracer for in vivo imaging of the dopamine D2 high-affinity state with positron emission tomography. Journal of Medicinal Chemistry, 48(12), 4153–4160.
CAS Article Google Scholar
Zangen, A., Roth, Y., Voller, B., & Hallett, M. (2005). Transcranial magnetic stimulation of deep brain regions: evidence for efficacy of the H-coil. Clinical Neurophysiology, 116(4), 775–779. https://doi.org/10.1016/j.clinph.2004.11.008.
Article PubMed Google Scholar

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Acknowledgements

The authors would like to thank Heather O’Leary and Annabel Fan for their assistance.

Funding

This work was funded by a research grant from the Campbell Family via the CAMH foundation fund (grant #200).

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Authors and Affiliations

Translational Addiction Research Laboratory, Campbell Family Mental Health Research Institute, Centre for Addiction and Mental Health (CAMH), 33 Russell Street, Toronto, ON, Canada, M5S 2S1
Saima Malik & Bernard Le Foll
Research Imaging Centre, Centre for Addiction and Mental Health, 250 College St, Toronto, ON, Canada
Mark Jacobs, Sang-Soo Cho, Isabelle Boileau, Alan Wilson & Antonio P. Strafella
Division of Brain, Imaging and Behaviour – Systems Neuroscience, Krembil Research Institute, University Health Network, University of Toronto, Toronto, ON, Canada
Mark Jacobs, Sang-Soo Cho & Antonio P. Strafella
Department of Psychiatry, University of Toronto, Toronto, ON, Canada
Daniel Blumberger, Zafiris J. Daskalakis & Bernard Le Foll
Temerty Centre for Therapeutic Brain Intervention, Centre for Addiction and Mental Health, 1001 Queen St, Toronto, ON, Canada
Daniel Blumberger & Zafiris J. Daskalakis
Campbell Family Mental Health Research Institute, Centre for Addiction and Mental Health, Toronto, ON, Canada
Daniel Blumberger, Zafiris J. Daskalakis & Bernard Le Foll
Center for Social and Affective Neuroscience, Department of Clinical and Experimental Medicine, Linköping University, S-581 83, Linköping, Sweden
Markus Heilig
Movement Disorder Unit & E.J. Safra Parkinson Disease Program, Toronto Western Hospital, University Health Network, University of Toronto, Toronto, ON, Canada
Antonio P. Strafella
Brain Stimulation and Behavior Lab, Ben Gurion University, POB 653, Beer-Sheva, 84105, Israel
Abraham Zangen
Addiction Medicine Service, Ambulatory Care and Structured Treatments, Centre for Addiction and Mental Health, 100 Stokes St, Toronto, ON, Canada
Bernard Le Foll

Authors

Saima Malik
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Mark Jacobs
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Sang-Soo Cho
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Isabelle Boileau
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Daniel Blumberger
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Markus Heilig
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Alan Wilson
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Zafiris J. Daskalakis
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Antonio P. Strafella
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Abraham Zangen
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Bernard Le Foll
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Corresponding author

Correspondence to Bernard Le Foll.

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Conflict of interest

Dr. Malik, Dr. Cho, Dr. Boileau, Dr. Strafella, Dr. Wilson, Dr. Heilig and Mark Jacobs reported no biomedical financial interests or potential conflicts of interest. Dr. Le Foll has received in-kind support from Brainsway that provided the equipment used in this study. In addition, Dr. Le Foll received in kind donation of drug supplies from Pfizer or GW-Pharma. He received grant and salary support for other unrelated studies from Pfizer Inc. and Bioprojet laboratory. Dr. Le Foll has been a consultant or has received honorariums for lectures from Richter Pharmaceuticals, Lundbeck, Mylan, Ethypharm, Metrum and Pfizer. Dr. Daskalakis has received research and equipment in-kind support for an investigator-initiated study through Brainsway Inc, and has also served on the advisory board for Sunovion, Hoffmann-La Roche Limited and Merck and received speaker support from Eli Lilly. Dr. Blumberger has received research support from the Canadian Institutes of Health Research (CIHR), National Institute of Health (NIH), Brain Canada and the Temerty Family through the Centre for Addiction and Mental Health (CAMH) Foundation and the Campbell Research Institute. He receives research support and in-kind equipment support for an investigator-initiated study from Brainsway Ltd. and he is the site principal investigator for three sponsor-initiated studies for Brainsway Ltd. He also receives in-kind equipment support from Magventure for an investigator-initiated study and receives medication supplies for an investigator-initiated trial from Invidior. Dr. Zangen is a co-inventor of the deep TMS H-coil system, serves as consultant for, and has financial interests in Brainsway.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

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Malik, S., Jacobs, M., Cho, SS. et al. Deep TMS of the insula using the H-coil modulates dopamine release: a crossover [¹¹C] PHNO-PET pilot trial in healthy humans. Brain Imaging and Behavior 12, 1306–1317 (2018). https://doi.org/10.1007/s11682-017-9800-1

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Published: 23 November 2017
Issue Date: October 2018
DOI: https://doi.org/10.1007/s11682-017-9800-1

Keywords

Insula
PET
Dopamine
H-coil
Deep rTMS
PHNO