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Theta Burst Stimulation of the Precuneus Modulates Resting State Connectivity in the Left Temporal Pole

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Abstract

It has been shown that continuous theta burst stimulation (cTBS) over the precuneus acts on specific memory retrieval abilities. In order to study the neural mechanisms beyond these findings, we combined cTBS and resting-state functional magnetic resonance imaging. Our experimental protocol involved stimulation and sham conditions on a group of healthy subjects, and each condition included a baseline and two follow-up acquisitions (5 and 15 min after baseline) after cTBS. We analysed brain functional connectivity by means of graph theoretical measures, with a specific focus on the network modular structure. Our results showed that cTBS of the precuneus selectively affects the left temporal pole, decreasing its functional connectivity in the first follow-up. Moreover, we observed a significant increase in the size of the module of the precuneus in the second follow-up. Such effects were absent in the sham condition. We observed here a modulation of functional connectivity as a result of inhibitory stimulation over the precuneus. Such a modulation first acts indirectly on the temporal area and then extends the connectivity of the precuneus itself by a feed-back mechanism. Our current findings extend our previous behavioural observations and increase our understanding of the mechanisms underlying the stimulation of the precuneus.

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Abbreviations

TMS:

Transcranial magnetic stimulation

fMRI:

Functional magnetic resonance imaging

cTBS:

Continuous theta burst stimulation

PC:

Precuneus

References

  • Achard S, Bullmore E (2007) Efficiency and cost of economical brain functional networks. PLoS Comput Biol 3(2) 174–183

    Article  CAS  Google Scholar 

  • Aertsen AM, Gerstein GL (1985) Evaluation of neuronal connectivity: sensitivity of cross-correlation. Brain Res 340:341–354

    Article  CAS  PubMed  Google Scholar 

  • Bassett DS, Wymbs NF, Porter MA, Mucha PJ, Carlson JM, Grafton ST (2011) Dynamic reconfiguration of human brain networks during learning. Proc Natl Acad Sci USA 108(18):7641–7646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bassett DS, Wymbs NF, Rombach MP, Porter MA, Mucha PJ Grafton ST (2013) Task-based core-periphery organisation of human brain dynamics. PLoS Comput Biol 9(9) 1–16

    Article  Google Scholar 

  • Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29(4):1165–1188

    Article  Google Scholar 

  • Blaizot X, Mansilla F, Insausti AM, Constans JM, Salinas-Alamán A, Pró-Sistiaga P, Mohedano-Moriano A, Insausti R (2010) The human parahippocampal region: I. Temporal pole cytoarchitectonic MRI correlation. Cereb Cortex 20(9):2198–2212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonnì S, Veniero D, Mastropasqua C, Ponzo V, Caltagirone C, Bozzali M, Koch G (2015) TMS evidence for a selective role of the precuneus in source memory retrieval. Behav Brain Res 282:70–75

    Article  PubMed  Google Scholar 

  • Braun U, Schaefer A, Walter H, Erk S, Romanczuk-Seiferth N, Haddad L, Schweiger J, Grimm O, Heinz A, Tost H, Meyer-Lindenberg A, Bassett DS (2015) Dynamic reconfiguration of frontal brain networks during executive cognition in humans. Proc Natl Acad Sci USA 112(37):11678–11683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10:186–198

    Article  CAS  PubMed  Google Scholar 

  • Bullmore E, Fadili J, Maxim V, Sendur L, Whitcher B, Suckling J, Brammer M, Breakspear M (2004) Wavelets and functional magnetic resonance imaging of the human brain. Neuroimage 23:S234–S249

    Article  PubMed  Google Scholar 

  • Cavanna AE, Trimble MR (2006) The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129:564–583

    Article  PubMed  Google Scholar 

  • Chai LR, Mattar MG, Blank IA, Fedorenko E, Bassett DS (2016) Functional network dynamics of the language system. Cereb Cortex 26(11):4148–4159

    Article  PubMed Central  Google Scholar 

  • Cocchi L, Sale MV, Lord A, Zalesky A, Breakspear M, Mattingley JB (2015) Dissociable effects of local inhibitory and excitatory theta-burst stimulation on large-scale brain dynamics. J Neurophysiol 113:3375–3385

    Article  PubMed  PubMed Central  Google Scholar 

  • Cocchi L, Sale MV, Gollo LL, Bell PT, Nguyen VT, Zalesky A, Breakspear M, Mattingley JB (2016) A hierarchy of timescales explains distinct effects of local inhibition of primary visual cortex and frontal eye fields. Elife 5:1–17

    Article  Google Scholar 

  • Cox RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29(3):162–173

    Article  CAS  PubMed  Google Scholar 

  • Daselaar SM, Prince SE, Dennis NA, Hayes SM, Kim H, Cabeza R (2009) Posterior midline and ventral parietal activity is associated with retrieval success and encoding failure. Front Hum Neurosci 3(13):1–10

    Google Scholar 

  • Deco G, Jirsa VK, McIntosh AR (2011) Emerging concepts for the dynamical organization of resting-state activity in the brain. Nat Rev Neurosci 12:43–56

    Article  CAS  PubMed  Google Scholar 

  • Desikan RS, Segonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31:968–980

    Article  PubMed  Google Scholar 

  • Donaldson DI, Wheeler ME, Petersen SE (2010) Remember the source: dissociating frontal and parietal contributions to episodic memory. J Cogn Neurosci 22(2):377–391

    Article  PubMed  Google Scholar 

  • Doron KW, Bassett DS, Gazzaniga MS (2012) Dynamic network structure of interhemispheric coordination. Proc Natl Acad Sci USA 109(46):18661–18668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fallani, FDV, Richiardi J, Chavez M, Achard S (2014) Graph analysis of functional brain networks: practical issues in translational neuroscience. Philos Trans R Soc B 369(1653):1–36

    Google Scholar 

  • Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33:341–355

    Article  CAS  PubMed  Google Scholar 

  • Fisher RA, (1935) The design of experiments. Hafner, New York

    Google Scholar 

  • Fornito A, Harrison BJ, Zalesky A, Simons JS (2012) Competitive and cooperative dynamics of large-scale brain functional networks supporting recollection. Proc Natl Acad Sci USA 109(31):12788–12793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700–711

    Article  CAS  PubMed  Google Scholar 

  • Fox MD, Halko MA, Eldaief MC, Pascual-Leone A (2012a) Measuring and manipulating brain connectivity with resting state functional connectivity magnetic resonance imaging (fcMRI) and transcranial magnetic stimulation (TMS). Neuroimage 62:2232–2243

    Article  PubMed  PubMed Central  Google Scholar 

  • Fox MD, Liu H, Pascual-Leone A (2012b) Identification of reproducible individualized targets for treatment of depression with TMS based on intrinsic connectivity. Neuroimage 66C:151–160

    Google Scholar 

  • Fox MD, Buckner RL, Liu H, Chakavarty MM, Lozano AM, Pascual-Leone A (2014) Resting-state networks link invasive and noninvasive brain stimulation across diverse psychiatric and neurological disease. Proc Natl Acad Sci USA 111(41):E4367–E4375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Friston KJ, Frith CD, Frackowiak RS (1993) Principal component analysis learning algorithms: a neurobiological analysis. Proc Biol Sci 254:47–54

    Article  CAS  PubMed  Google Scholar 

  • Gabrowsky TJ, Damasio H, Tranel D, Cooper GE, Ponto LLB Watkins GL, Hichwa RD (2003) Residual naming after damage to the left temporal pole: a PET activation study. Neuroimage 19:846–860

    Article  Google Scholar 

  • Gallassi R, Sambati L, Poda R, Maserati MS, Oppi F, Giulioni M, Tinuper P (2011) Accelerated long-term forgetting in temporal lobe epilepsy: evidence of improvement after left temporal pole lobectomy. Epilepsy Behav 22:793–795

    Article  PubMed  Google Scholar 

  • Gallos LK, Makse HA, Sigman M (2012) A small world of weak ties provides optimal global integration of self-similar modules in functional brain networks. Proc Natl Acad Sci USA 109(8):2825–2830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gratton C, Lee TG, Nomura EM, D’Esposito M (2013) The effect of theta-burst TMS on cognitive control networks measured with resting state fMRI. Front Syst Neurosci 7(124):1–14

    Google Scholar 

  • Guimerà R, Amaral LAN (2005) Functional cartography of complex metabolic networks. Nature 433:895–900

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC (2005) Theta burst stimulation of the human motor cortex. Neuron 45:201–206

    Article  CAS  PubMed  Google Scholar 

  • Huijbers W, Vannini P, Sperling RA, Pennartz CM, Cabeza R, Daselaar SM (2012) Explaining the encoding/retrieval flip: memory-related deactivations and activations in the posteromedial cortex. Neuropsychologia 50(14):3764–3774

    Article  CAS  PubMed  Google Scholar 

  • Hutchinson JB, Uncapher MR, Wagner AD (2009) Posterior parietal cortex and episodic retrieval: convergent and divergent effects of attention and memory. Learn Mem 16(6):343–356

    Article  PubMed  PubMed Central  Google Scholar 

  • Koch G, Del Olmo MF, Cheeran B et al (2007) Focal stimulation of the posterior parietal cortex increases the excitability of the ipsilateral motor cortex. J Neurosci 27:6815–6822

    Article  CAS  PubMed  Google Scholar 

  • Liston C, Chen AC, Zebley BD, Drysdale AT, Gordon R, Leuchter B, Voss HU, Casey BJ, Etkin A, Dubin MJ (2014) Default mode network mechanisms of transcranial magnetic stimulation in depression. Biol Psychiatry 76(7):517–526

    Article  PubMed  PubMed Central  Google Scholar 

  • Luft C, Pereda E, Banissy MJ, Bhattacharya J (2014) Best of both worlds: promise of combining brain stimulation and brain connectome. Front Syst Neurosci 8(132):1–15

    Google Scholar 

  • Maguire EA, Mummery CJ, Büchel C (2000) Patterns of hippocampal–cortical interaction dissociate temporal lobe memory subsystems. Hippocampus 10(4):475–482

    Article  CAS  PubMed  Google Scholar 

  • Mastropasqua C, Bozzali M, Ponzo V, Giulietti G, Caltagirone C, Cercignani M, Koch G (2014) Network based statistical analysis detects changes induced by continuous theta-burst stimulation on brain activity at rest. Front Psychiatry 5(97):1–7

    Google Scholar 

  • Newman MEJ (2006) Finding community structure in networks using the eigenvectors of matrices. Phys Rev E 74:1–22

    Article  Google Scholar 

  • Pobric G, Ralph MAL, Jeffries E (2009) The role of the anterior temporal lobes in the comprehension of concrete and abstract words: rTMS evidence. Cortex 45:1104–1110

    Article  PubMed  PubMed Central  Google Scholar 

  • Ranieri F, Ferraccioli M, Bassi MS, Musumeci G, Di Lazzaro V, Gainotti G, Marra C (2015) Familiarity for famous faces and names is not equally subtended by the right and left temporal poles: evidence from an rTMS study. Neurobiol Learn Mem 125:15–23

    Article  CAS  PubMed  Google Scholar 

  • Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52:1059–1069

    Article  PubMed  Google Scholar 

  • Sale MV, Mattingley JB, Zalesky A, Cocchi L (2015) Imaging human brain networks to improve the clinical efficacy of non-invasive brain stimulation. Neurosci Behav Rev 57:187–198

    Article  Google Scholar 

  • Serra, L., Mancini, M., Silvestri, G., et al., (2016a) Brain connectomics’ modification to clarify motor and nonmotor features of myotonic dystrophy type 1. Neural Plast. doi:10.1155/2016/2696085

    PubMed  PubMed Central  Google Scholar 

  • Serra L, Cercignani M, Bruschini M, Cipolotti L, Mancini M, Silvestri G et al (2016b) “I know that you know that I know”: neural substrates associated with social cognition deficits in DM1 patients. PLoS ONE 11(6):e0156901

    Article  PubMed  PubMed Central  Google Scholar 

  • Shipton OA, El-Gaby M, Apergis-Schoute J, Disseroth K, Bannerman DM, Paulsen O, Kohl MM (2014) Left-right dissociation of hippocampal memory processes in mice. Proc Natl Acad Sci USA 111(42):15238–15243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sporns O. (2015) Cerebral cartography and connectomics. Philos Trans B 370(1668): 1–12

    Article  Google Scholar 

  • Sporns O, Betzel RF (2016) Modular nrain networks. Annu Rev Psychol 67:613–640

    Article  PubMed  Google Scholar 

  • Stokes MG, Chambers CD, Gould IC, Henderson TR, Janko NE, Allen NB, Mattingley JB (2005) Simple metric for scaling motor threshold based on scalp-cortex distance: application to studies using transcranial magnetic stimulation. J Neurophysiol 94(6):4520–4527

    Article  PubMed  Google Scholar 

  • Turriziani P, Smirni D, Zappalà G, Mangano GR, Oliveri M, Cipolotti L (2012) Enhancing memory performance with rTMS in healthy subjects and individuals with Mild Cognitive Impairment: the role of the right dorsolateral prefrontal cortex. Front Hum Neurosci 6(62):1–8

    Google Scholar 

  • van Wijk, BCM, Stam, CJ, Daffertshofer, A, (2010) Comparing brain networks of different size and connectivity density using graph theory. PLoS ONE 5(10):1–13

    Google Scholar 

  • van den Heuvel MP, Hulshoff Pol HE (2010) Exploring the brain network: a review on resting-state fMRI functional connectivity. Eur Neuropsychopharmacol 20:519–534

    Article  PubMed  Google Scholar 

  • van den Heuvel MP, Sporns O (2011) Rich-club organization of the human connectome. J Neurosci 31(44):15775–15786

    Article  PubMed  Google Scholar 

  • van den Heuvel MP, Sporns O (2013a) Network hubs in the human brain. Trends Cogn Sci 17(12):683–696

    Article  PubMed  Google Scholar 

  • van den Heuvel MP, Sporns O (2013b) An anatomical substrate for integration among functional networks in human cortex. J Neurosci 33(36):14489–14500

    Article  PubMed  Google Scholar 

  • Wagner AD, Shannon BJ, Kahn L, Buckner RL (2005) Parietal lobe contributions to episodic memory retrieval. Trends Cogn Sci 9:445–453

    Article  PubMed  Google Scholar 

  • Zanto TP, Rubens MT, Thangavel A, Gazzaley A (2011) Causal role of the prefrontal cortex in top-down modulation of visual processing and working memory. Nat Neurosci 14:656–661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This study was funded by a grant from the Italian Ministry of Health (RF10.047) awarded to Marco Bozzali.

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Correspondence to Matteo Mancini.

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Mancini, M., Mastropasqua, C., Bonnì, S. et al. Theta Burst Stimulation of the Precuneus Modulates Resting State Connectivity in the Left Temporal Pole. Brain Topogr 30, 312–319 (2017). https://doi.org/10.1007/s10548-017-0559-x

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  • DOI: https://doi.org/10.1007/s10548-017-0559-x

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