Effects of Continuous Versus Intermittent Theta-burst TMS on FMRI Connectivity

Overview

Journal Front Hum Neurosci

Specialty Neurology

Date 2024 Jun 17

PMID 38883322

Authors

Molly S Hermiller

Affiliations

Soon will be listed here.

Abstract

Transcranial magnetic stimulation is a noninvasive technique that can be used to evoke distributed network-level effects. Previous work demonstrated that the Hippocampal-Cortical Network responds preferably (i.e., greater memory improvement and increases in hippocampal-network connectivity) to continuous theta-burst stimulation protocol relative to intermittent theta-burst and to 20-Hz rTMS. Here, these data were further analyzed to characterize effects of continuous versus intermittent theta-burst stimulation on network-level connectivity measures - as well as local connectedness - via resting-state fMRI. In contrast to theories that propose continuous and intermittent theta-burst cause local inhibitory versus excitatory effects, respectively, both protocols caused local decreases in fMRI connectivity around the stimulated parietal site. While iTBS caused decreases in connectivity across the hippocampal-cortical network, cTBS caused increases and decreases in connectivity across the network. cTBS had no effect on the parietal-cortical network, whereas iTBS caused decreases in the right parietal cortex (contralateral hemisphere to the stimulation target). These findings suggest that continuous theta-burst may have entrained the endogenous hippocampal-cortical network, whereas the intermittent train was unable to maintain entrainment that may have yielded the long-lasting effects measured in this study (i.e., within 20-min post-stimulation). Furthermore, these effects were specific to the hippocampal-cortical network, which has a putative endogenous functionally-relevant theta rhythm, and not to the parietal network. These results add to the growing body of evidence that suggests effects of theta-burst stimulation are not fully characterized by excitatory/inhibitory theories. Further work is required to understand local and network-level effects of noninvasive stimulation.

References

Lega B, Germi J, Rugg M . Modulation of Oscillatory Power and Connectivity in the Human Posterior Cingulate Cortex Supports the Encoding and Retrieval of Episodic Memories. J Cogn Neurosci. 2017; 29(8):1415-1432. DOI: 10.1162/jocn_a_01133. View

Kaplan R, Bush D, Bonnefond M, Bandettini P, Barnes G, Doeller C . Medial prefrontal theta phase coupling during spatial memory retrieval. Hippocampus. 2014; 24(6):656-65. PMC: 4028411. DOI: 10.1002/hipo.22255. View

Nee D, DEsposito M . The hierarchical organization of the lateral prefrontal cortex. Elife. 2016; 5. PMC: 4811776. DOI: 10.7554/eLife.12112. View

Berry S, Thompson R . Prediction of learning rate from the hippocampal electroencephalogram. Science. 1978; 200(4347):1298-300. DOI: 10.1126/science.663612. View

Anderson K, Rajagovindan R, Ghacibeh G, Meador K, Ding M . Theta oscillations mediate interaction between prefrontal cortex and medial temporal lobe in human memory. Cereb Cortex. 2009; 20(7):1604-12. DOI: 10.1093/cercor/bhp223. View

Hanslmayr S, Matuschek J, Fellner M . Entrainment of prefrontal beta oscillations induces an endogenous echo and impairs memory formation. Curr Biol. 2014; 24(8):904-9. DOI: 10.1016/j.cub.2014.03.007. View

Steinvorth S, Wang C, Ulbert I, Schomer D, Halgren E . Human entorhinal gamma and theta oscillations selective for remote autobiographical memory. Hippocampus. 2009; 20(1):166-73. DOI: 10.1002/hipo.20597. View

Riddle J, Hwang K, Cellier D, Dhanani S, DEsposito M . Causal Evidence for the Role of Neuronal Oscillations in Top-Down and Bottom-Up Attention. J Cogn Neurosci. 2019; 31(5):768-779. PMC: 6701188. DOI: 10.1162/jocn_a_01376. View

Foster B, Kaveh A, Dastjerdi M, Miller K, Parvizi J . Human retrosplenial cortex displays transient theta phase locking with medial temporal cortex prior to activation during autobiographical memory retrieval. J Neurosci. 2013; 33(25):10439-46. PMC: 3685837. DOI: 10.1523/JNEUROSCI.0513-13.2013. View

10.

Di Lazzaro V, Dileone M, Pilato F, Capone F, Musumeci G, Ranieri F . Modulation of motor cortex neuronal networks by rTMS: comparison of local and remote effects of six different protocols of stimulation. J Neurophysiol. 2011; 105(5):2150-6. DOI: 10.1152/jn.00781.2010. View

11.

Squire L . The medial temporal lobe memory system. Science. 1991; 253(5026):1380-6. DOI: 10.1126/science.1896849. View

12.

Pascual-Leone A, Valls-Sole J, Wassermann E, Hallett M . Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain. 1994; 117 ( Pt 4):847-58. DOI: 10.1093/brain/117.4.847. View

13.

Zhang H, Jacobs J . Traveling Theta Waves in the Human Hippocampus. J Neurosci. 2015; 35(36):12477-87. PMC: 4563037. DOI: 10.1523/JNEUROSCI.5102-14.2015. View

14.

Weinrich C, Brittain J, Nowak M, Salimi-Khorshidi R, Brown P, Stagg C . Modulation of Long-Range Connectivity Patterns via Frequency-Specific Stimulation of Human Cortex. Curr Biol. 2017; 27(19):3061-3068.e3. PMC: 5640151. DOI: 10.1016/j.cub.2017.08.075. View

15.

Romei V, Thut G, Silvanto J . Information-Based Approaches of Noninvasive Transcranial Brain Stimulation. Trends Neurosci. 2016; 39(11):782-795. DOI: 10.1016/j.tins.2016.09.001. View

16.

Thut G, Schyns P, Gross J . Entrainment of perceptually relevant brain oscillations by non-invasive rhythmic stimulation of the human brain. Front Psychol. 2011; 2:170. PMC: 3142861. DOI: 10.3389/fpsyg.2011.00170. View

17.

Mufson E, Pandya D . Some observations on the course and composition of the cingulum bundle in the rhesus monkey. J Comp Neurol. 1984; 225(1):31-43. DOI: 10.1002/cne.902250105. View

18.

Lin J, Rugg M, Das S, Stein J, Rizzuto D, Kahana M . Theta band power increases in the posterior hippocampus predict successful episodic memory encoding in humans. Hippocampus. 2017; 27(10):1040-1053. PMC: 6517838. DOI: 10.1002/hipo.22751. View

19.

Valchev N, Curcic-Blake B, Renken R, Avenanti A, Keysers C, Gazzola V . cTBS delivered to the left somatosensory cortex changes its functional connectivity during rest. Neuroimage. 2015; 114:386-397. PMC: 4968652. DOI: 10.1016/j.neuroimage.2015.04.017. View

20.

Chanes L, Quentin R, Tallon-Baudry C, Valero-Cabre A . Causal frequency-specific contributions of frontal spatiotemporal patterns induced by non-invasive neurostimulation to human visual performance. J Neurosci. 2013; 33(11):5000-5. PMC: 6618994. DOI: 10.1523/JNEUROSCI.4401-12.2013. View