- Published: January 16, 2022
- Updated: January 16, 2022
- University / College: Dalhousie University
- Language: English
- Downloads: 28
Repetitive transcranial magnetic stimulation (rTMS) is a non-invasive brain neuromodulation approach, which has demonstrated clinical efficacy for major depressive disorder, obsessive-compulsive disorder, stroke, and substance use disorders ( Mantovani et al., 2006 ; O’Reardon et al., 2007 ; Ludemann-Podubecka et al., 2015 ; Shen et al., 2016 ). In addition, rTMS intervention could enhance cognitive performance (e. g., inhibit control, decision making, working memory) in healthy individuals when targeting relative networks ( Bagherzadeh et al., 2016 ; Rahnev et al., 2016 ; Lowe et al., 2018 ). One important neural mechanism underlying these efficacy was the cortical plasticity induced from the rTMS stimulation.
Previous studies uncovered potential gender differences in rTMS induced cortical plasticity. The study conducted by Inghilleri and colleagues revealed ovarian hormones dependent effect of primary motor cortex (M1) excitability is present in females, whereas this is not present in males ( Inghilleri et al., 2004 ). The results indicated that females showed higher rTMS induced motor evoked potential (MEP) in the late menstrual cycle, which is consistent with the study by Smith and his colleagues ( Smith et al., 1999 , 2002 ). However, the difference of cortical excitability induced by TMS in male and female was not been found in young adulthood in other studies, but age-related cortical excitability discrepancy within gender shows that females progress more reduction of excitability in elderly age compared to male ( Sella et al., 2014 ; Polimanti et al., 2016 ). One reason for the absence of plasticity gender difference in young adulthood was that the menstrual cycle of female subjects was not considered. TMS could alter cognitive performance; females displayed reduced smile face mimicry and perception, after targeted in the right M1 and the right primary somatosensory cortex with continuous theta burst stimulation (cTBS), compared to targeted in the vertex, whereas males showed no TMS effects ( Korb et al., 2015 ). In terms of chronic treatment effects, a meta-analysis of rTMS on major depression patients revealed a dependency effect of sex, showing that females have higher response to treatment ( Kedzior et al., 2014 ). However, it is unclear whether rTMS treatment yields a comparable gender difference in drug abuse populations.
TMS induced cortical plasticity discrepancy in male and female rarely studied, it is unclear whether male and female respond equally to TMS. Two pilot studies for cocaine dependents included two females in 18 subjects and one female in 18 subjects ( Bolloni et al., 2016 ; Martinez et al., 2018 ), respectively. This defect was solved in a recent study, which reported rTMS suppresses craving in a group of female methamphetamine dependents ( Liu et al., 2018 ). The group of female methamphetamine dependents were treated by 10 Hz rTMS stimulation in the left dorsolateral prefrontal cortex (DLPFC), for a duration of 20 times in 4 weeks with 2000 pulses single session. The results showed that the cue-induced craving score significantly decreased in the treated group, compared to the untreated group, with lasting effects until another month in follow-up. The study sufficiently demonstrated the effectiveness of craving reduction in female groups with rTMS, which is consistent with the male groups ( Liu et al., 2017 ).
One priority for future research from the present study is to include the menstrual cycle of female dependents, which is inevitably included in 1-month course of treatment. Females have a higher sensitivity for cocaine in the follicular phase, and attenuate in the luteal phase ( Bobzean et al., 2014 ). It may be regulated by progesterone levels, which are consistent with cortical plasticity induced by paired TMS and more inhibition in the luteal phase (high progesterone level) compared to the follicular phase (low progesterone level) ( Smith et al., 1999 ). Individual genotypes would probably be tested before treatment in the future. For instance, the Val66Met (a type of brain-derived neurotrophic factor gene) carry an individual response unstable to TMS compared to Val66Val individuals ( Cheeran et al., 2008 ). Another factor has been ignored is response rate to non-invasive brain stimulation (NIBS) in subjects, and the number that has been confirmed is 40% ( Lopez-Alonso et al., 2014 ).
One limitation of the study is that it excludes the involvement of a male group. Male and female subjects have difference in reasons of using drugs, addictive behavior, and peaking of craving progress. In the initial stage, men’s drug intake is more influenced by their peers, while women’s drug intake is more related to their mental state ( Becker and Chartoff, 2019 ). Female drug users alter from casual use to compulsive use more rapidly than males, and have a higher craving for drugs and relapse ( Bobzean et al., 2014 ). Moreover, females progress more mental health symptoms during treatment. These are also important factors influencing treatment effects. Another limitation the lack of longer follow-ups (e. g., relapse, craving). The author conducted a 2 month follow-up in the present study, and found that the treatment effect was still valid ( Liu et al., 2018 ). It is insufficient to assess the treatment effect of TMS for substance dependents, especially when the treatment effectiveness may differ in males and females.
In short, the present study demonstrated that rTMS can also reduce the craving of female methamphetamine dependents. In the future, we need to re-evaluate the similarities and differences between gender differences in treatment and brain function assessment by more clinical, cognitive and physiological indicators and protocols.
Author Contributions
YZ drafted the manuscript. YZ and HZ revised it. WH was in charge for the final version. All authors read and approved the submitted version.
Funding
This work was supported by the National Natural Science Foundation of China (Grant Nos. 31970991 and 81601166).
Conflict of Interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
References
Bagherzadeh, Y., Khorrami, A., Zarrindast, M. R., Shariat, S. V., and Pantazis, D. (2016). Repetitive transcranial magnetic stimulation of the dorsolateral prefrontal cortex enhances working memory. Exp. Brain Res. 234, 1807–1818. doi: 10. 1007/s00221-016-4580-1
PubMed Abstract | CrossRef Full Text | Google Scholar
Becker, J. B., and Chartoff, E. (2019). Sex differences in neural mechanisms mediating reward and addiction. Neuropsychopharmacology 44, 166–183. doi: 10. 1038/s41386-018-0125-6
PubMed Abstract | CrossRef Full Text | Google Scholar
Bobzean, S. A. M., DeNobrega, A. K., and Perrotti, L. I. (2014). Sex differences in the neurobiology of drug addiction. Exp. Neurol. 259, 64–74. doi: 10. 1016/j. expneurol. 2014. 01. 022
PubMed Abstract | CrossRef Full Text | Google Scholar
Bolloni, C., Panella, R., Pedetti, M., Frascella, A. G., Gambelunghe, C., Piccoli, T., et al. (2016). Bilateral transcranial magnetic stimulation of the prefrontal cortex reduces cocaine intake: a pilot study. Front. Psychiatry 7: 133. doi: 10. 3389/fpsyt. 2016. 00133
PubMed Abstract | CrossRef Full Text | Google Scholar
Cheeran, B., Talelli, P., Mori, F., Koch, G., Suppa, A., Edwards, M., et al. (2008). A common polymorphism in the brain-derived neurotrophic factor gene (BDNF) modulates human cortical plasticity and the response to rTMS. J. Physiol. 586, 5717–5725. doi: 10. 1113/jphysiol. 2008. 159905
PubMed Abstract | CrossRef Full Text | Google Scholar
Inghilleri, M., Conte, A., Curra, A., Frasca, V., Lorenzano, C., and Berardelli, A. (2004). Ovarian hormones and cortical excitability. An rTMS study in humans. Clin. Neurophysiol. 115, 1063–1068. doi: 10. 1016/j. clinph. 2003. 12. 003
PubMed Abstract | CrossRef Full Text | Google Scholar
Kedzior, K. K., Azorina, V., and Reitz, S. K. (2014). More female patients and fewer stimuli per session are associated with the short-term antidepressant properties of repetitive transcranial magnetic stimulation (rTMS): a meta-analysis of 54 sham-controlled studies published between 1997-2013. Neuropsychiatr. Dis. Treat. 10, 727–756. doi: 10. 2147/Ndt. S58405
PubMed Abstract | CrossRef Full Text | Google Scholar
Korb, S., Malsert, J., Rochas, V., Rihs, T. A., Rieger, S. W., Schwab, S., et al. (2015). Gender differences in the neural network of facial mimicry of smiles–An rTMS study. Cortex 70, 101–114. doi: 10. 1016/j. cortex. 2015. 06. 025
PubMed Abstract | CrossRef Full Text | Google Scholar
Liu, Q., Shen, Y., Cao, X., Li, Y., Chen, Y., Yang, W., et al. (2017). Either at left or right, both high and low frequency rTMS of dorsolateral prefrontal cortex decreases cue induced craving for methamphetamine. Am. J. Addict. 26, 776–779. doi: 10. 1111/ajad. 12638
CrossRef Full Text | Google Scholar
Liu, T., Li, Y., Shen, Y., Liu, X., and Yuan, T. F. (2018). Gender does not matter: add-on repetitive transcranial magnetic stimulation treatment for female methamphetamine dependents. Prog. Neuropsychopharmacol. Biol. Psychiatry 92, 70–75. doi: 10. 1016/j. pnpbp. 2018. 12. 018
CrossRef Full Text | Google Scholar
Lopez-Alonso, V., Cheeran, B., Rio-Rodriguez, D., and Fernandez-Del-Olmo, M. (2014). Inter-individual variability in response to non-invasive brain stimulation paradigms. Brain Stimul. 7, 372–380. doi: 10. 1016/j. brs. 2014. 02. 004
PubMed Abstract | CrossRef Full Text | Google Scholar
Lowe, C. J., Manocchio, F., Safati, A. B., and Hall, P. A. (2018). The effects of theta burst stimulation (TBS) targeting the prefrontal cortex on executive functioning: a systematic review and meta-analysis. Neuropsychologia 111, 344–359. doi: 10. 1016/j. neuropsychologia. 2018. 02. 004
PubMed Abstract | CrossRef Full Text | Google Scholar
Ludemann-Podubecka, J., Bosl, K., and Nowak, D. A. (2015). Repetitive transcranial magnetic stimulation for motor recovery of the upper limb after stroke. Prog. Brain Res. 218, 281–311. doi: 10. 1016/bs. pbr. 2014. 12. 001
PubMed Abstract | CrossRef Full Text | Google Scholar
Mantovani, A., Lisanby, S. H., Pieraccini, F., Ulivelli, M., Castrogiovanni, P., and Rossi, S. (2006). Repetitive transcranial magnetic stimulation (rTMS) in the treatment of obsessive-compulsive disorder (OCD) and Tourette’s syndrome (TS). Int. J. Neuropsychopharmacol. 9, 95–100. doi: 10. 1017/S1461145705005729
PubMed Abstract | CrossRef Full Text | Google Scholar
Martinez, D., Urban, N., Grassetti, A., Chang, D., Hu, M. C., Zangen, A., et al. (2018). Transcranial magnetic stimulation of medial prefrontal and cingulate cortices reduces cocaine self-administration: a pilot study. Front. Psychiatry 9: 80. doi: 10. 3389/fpsyt. 2018. 00080
PubMed Abstract | CrossRef Full Text | Google Scholar
O’Reardon, J. P., Solvason, H. B., Janicak, P. G., Sampson, S., Isenberg, K. E., Nahas, Z., et al. (2007). Efficacy and safety of transcranial magnetic stimulation in the acute treatment of major depression: a multisite randomized controlled trial. Biol. Psychiatry 62, 1208–1216. doi: 10. 1016/j. biopsych. 2007. 01. 018
PubMed Abstract | CrossRef Full Text | Google Scholar
Polimanti, R., Simonelli, I., Zappasodi, F., Ventriglia, M., Pellicciari, M. C., Benussi, L., et al. (2016). Biological factors and age-dependence of primary motor cortex experimental plasticity. Neurol. Sci. 37, 211–218. doi: 10. 1007/s10072-015-2388-6
PubMed Abstract | CrossRef Full Text | Google Scholar
Rahnev, D., Nee, D. E., Riddle, J., Larson, A. S., and D’Esposito, M. (2016). Causal evidence for frontal cortex organization for perceptual decision making. Proc. Natl. Acad. Sci. U. S. A. 113, 6059–6064. doi: 10. 1073/pnas. 1522551113
PubMed Abstract | CrossRef Full Text | Google Scholar
Sella, O., Jones, R. D., and Huckabee, M. L. (2014). Age and gender effects on submental motor-evoked potentials. Age 36: 9735. doi: 10. 1007/s11357-014-9735-z
PubMed Abstract | CrossRef Full Text | Google Scholar
Shen, Y., Cao, X., Tan, T., Shan, C., Wang, Y., Pan, J., et al. (2016). 10-Hz repetitive transcranial magnetic stimulation of the left dorsolateral prefrontal cortex reduces heroin cue craving in long-term addicts. Biol. Psychiatry 80, e13–e14. doi: 10. 1016/j. biopsych. 2016. 02. 006
PubMed Abstract | CrossRef Full Text | Google Scholar
Smith, M. J., Adams, L. F., Schmidt, P. J., Rubinow, D. R., and Wassermann, E. M. (2002). Effects of ovarian hormones on human cortical excitability. Ann. Neurol. 51, 599–603. doi: 10. 1002/ana. 10180
PubMed Abstract | CrossRef Full Text | Google Scholar
Smith, M. J., Keel, J. C., Greenberg, B. D., Adams, L. F., Schmidt, P. J., Rubinow, D. A., et al. (1999). Menstrual cycle effects on cortical excitability. Neurology 53, 2069–2072. doi: 10. 1212/Wnl. 53. 9. 2069
PubMed Abstract | CrossRef Full Text | Google Scholar