Abstract
An increasing body of evidence points to the involvement of the cerebellum in cognition. Specifically, previous studies have shown that the superior and inferior portions of the cerebellum are involved in different verbal working memory (WM) mechanisms as part of two separate cerebro-cerebellar loops for articulatory rehearsal and phonological storage mechanisms. In comparison, our understanding of the involvement of the cerebellum in visual WM remains limited. We have previously shown that performance in verbal WM is disrupted by single-pulse transcranial magnetic stimulation (TMS) of the right superior cerebellum. The present study aimed to expand on this notion by exploring whether the inferior cerebellum is similarly involved in visual WM. Here, we used fMRI-guided, double-pulse TMS to probe the necessity of left superior and left inferior cerebellum in visual WM. We first conducted an fMRI localizer using the Sternberg visual WM task, which yielded targets in left superior and inferior cerebellum. Subsequently, TMS stimulation of these regions at the end of the encoding phase resulted in decreased accuracy in the visual WM task. Differences in the visual WM deficits caused by stimulation of superior and inferior left cerebellum raise the possibility that these regions are involved in different stages of visual WM.
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References
Anderson EJ, Mannan SK, Rees G, Sumner P, Kennard C. Overlapping functional anatomy for working memory and visual search. Exp Brain Res. 2010;200(1):91–107. https://doi.org/10.1007/s00221-009-2000-5.
Baddeley A. Working Memory. Curr Biol. 2010;20(4):136–40.
Baier B, Dieterich M, Stoeter P, Birklein F, Muller NG. Anatomical correlate of impaired covert visual attentional processes in patients with cerebellar lesions. J Neurosci. 2010;30(10):3770–6. https://doi.org/10.1523/JNEUROSCI.0487-09.2010.
Brissenden JA, Levin EJ, Osher DE, Halko MA, Somers DC. Functional evidence for a cerebellar node of the dorsal attention network. J Neurosci. 2016;36(22):6083–96. https://doi.org/10.1523/JNEUROSCI.0344-16.2016.
Brissenden JA, Somers DC. Cortico–cerebellar networks for visual attention and working memory. Curr Opin Psychol. 2019;29:239–47. https://doi.org/10.1016/j.copsyc.2019.05.003.
Brissenden JA, Tobyne SM, Halko MA, Somers DC. Stimulus-specific visual working memory representations in human cerebellar lobule VIIb/VIIIa. J Neurosci. 2021;41(5):1033–45. https://doi.org/10.1523/JNEUROSCI.1253-20.2020.
Brissenden JA, Tobyne SM, Osher DE, Levin EJ, Halko MA, Somers DC. Topographic cortico-cerebellar networks revealed by visual attention and working memory. Curr Biol. 2018;28(21):3364-3372.e5. https://doi.org/10.1016/j.cub.2018.08.059.
Buckner RL, Krienen FM, Castellanos A, Diaz JC, Yeo BTT. The organization of the human cerebellum estimated by intrinsic functional connectivity. J Neurophysiol. 2011;106(5):2322–45. https://doi.org/10.1152/jn.00339.2011.
Chen SHA, Desmond JE. Temporal dynamics of cerebro-cerebellar network recruitment during a cognitive task. Neuropsychologia. 2005;43(9):1227–37. https://doi.org/10.1016/j.neuropsychologia.2004.12.015.
Corbetta M, Akbudak E, Conturo TE, Snyder AZ, Ollinger JM, Drury HA, Linenweber MR, Petersen SE, Raichle ME, Van Essen DC, Shulman GL. A common network of functional areas for attention and eye movements. Neuron. 1998;21(4):761–73. https://doi.org/10.1016/S0896-6273(00)80593-0.
Corbetta M, Shulman GL. Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci. 2002;3(3):201–15. https://doi.org/10.1038/nrn755.
Corbin L, Marquer J. Is Sternberg’s memory scanning task really a short-term memory task? Swiss J Psychol. 2013;72(4):181–96. https://doi.org/10.1024/1421-0185/a000112.
Deng Z-D, Lisanby SH, Peterchev AV. Electric field depth–focality tradeoff in transcranial magnetic stimulation: simulation comparison of 50 coil designs. Brain Stimul. 2013;6(1):1–13. https://doi.org/10.1016/j.brs.2012.02.005.
Desmond JE, Chen SHA, Shieh PB. Cerebellar transcranial magnetic stimulation impairs verbal working memory. Ann Neurol. 2005;58(4):553–60. https://doi.org/10.1002/ana.20604.
Desmond JE, Gabrieli JDE, Wagner AD, Ginier BL, Glover GH. Lobular patterns of cerebellar activation in verbal working-memory and finger-tapping tasks as revealed by functional MRI. J Neurosci. 1997;17(24):9675–85. https://doi.org/10.1523/JNEUROSCI.17-24-09675.1997.
E K-H Chen, S.-H. A., Ho M-HR, Desmond JE. A meta-analysis of cerebellar contributions to higher cognition from PET and fMRI studies: a meta-analysis of cerebellar contributions. Hum Brain Mapp. 2014;35(2):593-615. https://doi.org/10.1002/hbm.22194
Elliott R, Dolan RJ. Differential neural responses during performance of matching and nonmatching to sample tasks at two delay intervals. J Neurosci. 1999;19(12):5066–73. https://doi.org/10.1523/JNEUROSCI.19-12-05066.1999.
Faul F, Erdfelder E, Lang A-G, Buchner A. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007;39:175–91.
Gottwald B. Evidence for distinct cognitive deficits after focal cerebellar lesions. J Neurol Neurosurg Psychiatry. 2004;75(11):1524–31. https://doi.org/10.1136/jnnp.2003.018093.
Guell X, Schmahmann J. Cerebellar functional anatomy: a didactic summary based on human fMRI evidence. Cerebellum. 2020;19(1):1–5. https://doi.org/10.1007/s12311-019-01083-9.
Hagler DJ, Sereno MI. Spatial maps in frontal and prefrontal cortex. Neuroimage. 2006;29(2):567–77. https://doi.org/10.1016/j.neuroimage.2005.08.058.
Herwig U. Spatial congruence of neuronavigated transcranial magnetic stimulation and functional neuroimaging. Clin Neurophysiol. 2002;113(4):462–8. https://doi.org/10.1016/S1388-2457(02)00026-3.
Hoang DH, Pagnier A, Cousin E, Guichardet K, Schiff I, Icher C, Dilharreguy B, Grill J, Frappaz D, Berger C, Schneider F, Dubois-Teklali F, Krainik A. Anatomo-functional study of the cerebellum in working memory in children treated for medulloblastoma. J Neuroradiol. 2019;46(3):207–13. https://doi.org/10.1016/j.neurad.2019.01.093.
Ito M. Cerebellum and neural control. Raven Press; 1984.
Jonides J, Smith EE, Marshuetz C, Koeppe RA, Reuter-Lorenz PA. Inhibition in verbal working memory revealed by brain activation. Proc Natl Acad Sci. 1998;95(14):8410–3. https://doi.org/10.1073/pnas.95.14.8410.
Kammer T, Beck S, Thielscher A, Laubis-Herrmann U, Topka H. Motor thresholds in humans: a transcranial magnetic stimulation study comparing different pulse waveforms, current directions and stimulator types. Clin Neurophysiol. 2001;112(2):250–8. https://doi.org/10.1016/S1388-2457(00)00513-7.
Liu T, Hospadaruk L, Zhu DC, Gardner JL. Feature-specific attentional priority signals in human cortex. J Neurosci. 2011;31(12):4484–95. https://doi.org/10.1523/JNEUROSCI.5745-10.2011.
Mayer JS, Bittner RA, Nikolić D, Bledowski C, Goebel R, Linden DEJ. Common neural substrates for visual working memory and attention. Neuroimage. 2007;36(2):441–53. https://doi.org/10.1016/j.neuroimage.2007.03.007.
Ng HBT, Kao K-LC, Chan YC, Chew E, Chuang KH, Chen SHA. Modality specificity in the cerebro-cerebellar neurocircuitry during working memory. Behav Brain Res. 2016;305:164–73. https://doi.org/10.1016/j.bbr.2016.02.027.
Oh S-H, Kim M-S. The role of spatial working memory in visual search efficiency. Psychon Bull Rev. 2004;11(2):275–81. https://doi.org/10.3758/BF03196570.
Pascual-Leone A. Transcranial magnetic stimulation in cognitive neuroscience – virtual lesion, chronometry, and functional connectivity. Curr Opin Neurobiol. 2000;10(2):232–7. https://doi.org/10.1016/S0959-4388(00)00081-7.
Paus T.. Combination of transcranial magnetic stimulation with brain imaging. In T. Mazziotta, J. A. (Ed.), Brain Mapping: The Methods (2nd ed., pp. 691–705). Academic Press, 2002.
Paus T, Jech R, Thompson CJ, Comeau R, Peters T, Evans AC. Transcranial magnetic stimulation during positron emission tomography: a new method for studying connectivity of the human cerebral cortex. J Neurosci. 1997;17(9):3178–84. https://doi.org/10.1523/JNEUROSCI.17-09-03178.1997.
Paus T, Wolforth M. Transcranial magnetic stimulation during PET: Reaching and verifying the target site. 4. 1998.
Peters T, Davey B, Munger P, Comeau R, Evans A. Three-dimensional multimodal image-guidance for neurosurgery. IEEE Trans Med Imaging. 1996;15(2):8.
Peterson MS, Kramer AF, Wang RF, Irwin DE, McCarley JS. Visual search has memory. Psychol Sci. 2001;12(4):287–92. https://doi.org/10.1111/1467-9280.00353.
Rac-Lubashevsky R, Kessler Y. Decomposing the n-back task: An individual differences study using the reference-back paradigm. Neuropsychologia. 2016;90:190–9. https://doi.org/10.1016/j.neuropsychologia.2016.07.013.
Ravizza SM, McCormick CA, Schlerf JE, Justus T, Ivry RB, Fiez JA. Cerebellar damage produces selective deficits in verbal working memory. Brain. 2006;129(2):306–20. https://doi.org/10.1093/brain/awh685.
Riva D, Giorgi C. The cerebellum contributes to higher functions during development: evidence from a series of children surgically treated for posterior fossa tumours. Brain J Neurol. 2000;123(Pt 5):1051–1061. https://doi.org/10.1093/brain/123.5.1051
Rushworth MFS, Ellison A, Walsh V. Complementary localization and lateralization of orienting and motor attention. Nat Neurosci. 2001;4(6):656–61. https://doi.org/10.1038/88492.
Salmi J, Pallesen KJ, Neuvonen T, Brattico E, Korvenoja A, Salonen O, Carlson S. Cognitive and motor loops of the human cerebro-cerebellar system. J Cogn Neurosci. 2010;22(11):2663–76. https://doi.org/10.1162/jocn.2009.21382.
Sheu Y-S, Liang Y, Desmond JE. Disruption of cerebellar prediction in verbal working memory. Front Hum Neurosci. 2019;13. https://doi.org/10.3389/fnhum.2019.00061
Smith EE, Jonides J. Storage and executive processes in the frontal lobes. 1999;283:5.
Sobczak-Edmans M, Ng THB, Chan YC, Chew E, Chuang KH, Chen SHA. Temporal dynamics of visual working memory. Neuroimage. 2016;124:1021–30. https://doi.org/10.1016/j.neuroimage.2015.09.038.
Sternberg S. High-speed scanning in human memory. Sci New Ser. 1966;153(3736):652–4.
Tomlinson SP, Davis NJ, Morgan HM, Bracewell RM. Cerebellar contributions to spatial memory. Neurosci Lett. 2014;578:182–6. https://doi.org/10.1016/j.neulet.2014.06.057.
Townsend J, Courchesne E, Covington J, Westerfield M, Harris NS, Lyden P, Lowry TP, Press GA. Spatial attention deficits in patients with acquired or developmental cerebellar abnormality. J Neurosci. 1999;19(13):5632–43. https://doi.org/10.1523/JNEUROSCI.19-13-05632.1999.
Treisman AM, Gelade G. A feature-integration theory of attention. Cogn Psychol. 1980;12(1):97–136. https://doi.org/10.1016/0010-0285(80)90005-5.
Veltman DJ, Rombouts SARB, Dolan RJ. Maintenance versus manipulation in verbal working memory revisited: an fMRI study. Neuroimage. 2003;18(2):247–56. https://doi.org/10.1016/S1053-8119(02)00049-6.
Yeh Y-Y, Kuo B-C, Liu H-L. The neural correlates of attention orienting in visuospatial working memory for detecting feature and conjunction changes. Brain Res. 2007;1130:146–57. https://doi.org/10.1016/j.brainres.2006.10.065.
Acknowledgements
The authors would like to especially thank Wei Peng Teo and Kai-Ling Cathy Kao for their contributions to running parts of the experiments and initial data analyses for the present work.
Funding
This work was supported by a Tier 2 research grant from the Ministry of Education, Singapore (MOE2011-T2-1–031). NV-G was supported by Singapore’s National Research Foundation (NRF) under the Science of Learning grant (NRF2016-SOL002-011). JED was supported by National Institutes of Health (NIH) grants R01 MH104588 and P50 HD103538.
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Nestor Viñas-Guasch and Tommy Hock Beng Ng contributed equally to this paper.
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Viñas-Guasch, N., Ng, T.H.B., Heng, J.G. et al. Cerebellar Transcranial Magnetic Stimulation (TMS) Impairs Visual Working Memory. Cerebellum 22, 332–347 (2023). https://doi.org/10.1007/s12311-022-01396-2
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DOI: https://doi.org/10.1007/s12311-022-01396-2