Skip to main content
SpringerLink
Log in

Cortical Connections Between Dorsal and Ventral Visual Streams in Humans: Evidence by TMS/EEG Co-Registration

  • Original Paper
  • Published:
Brain Topography Aims and scope Submit manuscript

Abstract

Parietal cortex subserves various cognitive tasks, ranging from attention to visuo-motor skills. It is part of a parieto-frontal network involved in attention, and part of the visual dorsal stream, opposed to the visual ventral stream, although increasing evidence suggests interchange of information between them. In this study, co-registration of Transcranial Magnetic Stimulation (TMS) and Electroencephalographic activity (EEG) has been used to investigate the spreading of cortical connections from the parietal cortex in healthy volunteers. TMS on the left parietal cortex activated a network of prefrontal regions in the contra-lateral hemisphere in a time range of 102–167 ms after the stimulus. Moreover, activation in the ipsi-lateral middle temporal and fusiform gyri was observed at 171–177 ms after delivery of TMS. Findings suggest the existence of late driven connections between parietal and prefrontal regions that could partially represent the neural pathway related to attention, even if, in this experiment, no attentional processing was requested. Late connections between dorsal and ventral streams were also evident, confirming previous evidence about interchange of information between them. Conclusively, the present investigation confirms that a great amount of information spreads from parietal cortex to different regions in the brain, supporting the idea that connections are more complex and articulated than those proposed. Present findings also suggest that the simultaneous recording of EEG during the application of TMS is a promising tool for the study of connections in the brain.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abe T, Ogawa K, Nittono H, Hori T (2008) Neural generators of brain potentials before rapid eye movements during human REM sleep: a study using sLORETA. Clin Neurophysiol 119:2044–2053

    Article  PubMed  Google Scholar 

  • Babiloni C, Vecchio F, Miriello M, Romani GL, Rossini PM (2006) Visuo-spatial consciousness and parieto-occipital areas: a high-resolution EEG study. Cereb Cortex 16:37–46

    Article  PubMed  Google Scholar 

  • Berndt I, Franz VH, Bülthoff HH, Wascher E (2002) Effects of pointing direction and direction predictability on event-related lateralizations of the EEG. Hum Mov Sci 21:387–410

    Article  PubMed  Google Scholar 

  • Borra E, Belmalih A, Calzavara R, Gerbella M, Murata A, Rozzi S, Luppino G (2008) Cortical connections of the macaque anterior intraparietal (AIP) area. Cereb Cortex 18:1094–1111

    Article  PubMed  Google Scholar 

  • Brignani D, Manganotti P, Rossini PM, Miniussi C (2008) Modulation of cortical oscillatory activity during transcranial magnetic stimulation. Hum Brain Mapp 29:603–612

    Article  PubMed  Google Scholar 

  • Bruno N, Bernardis P, Gentilucci M (2008) Visually guided pointing, the Müller-Lyer illusion, and the functional interpretation of the dorsal-ventral split: conclusions from 33 independent studies. Neurosci Biobehav Rev 32:423–437

    Article  PubMed  Google Scholar 

  • Bundesen C, Larsen A, Kyllingsbaek S, Paulson OB, Law I (2002) Attentional effects in the visual pathways: a whole-brain PET study. Exp Brain Res 147:394–406

    Article  PubMed  Google Scholar 

  • Busan P, Barbera C, Semenic M, Monti F, Pizzolato G, Pelamatti G, Battaglini PP (2009) Effect of Transcranial Magnetic Stimulation (TMS) on parietal and premotor cortex during planning of reaching movements. PLoS ONE 4:e4621

    Article  PubMed  Google Scholar 

  • Cavina-Pratesi C, Goodale MA, Culham JC (2007) FMRI reveals a dissociation between grasping and perceiving the size of real 3D objects. PLoS ONE 2:e424

    Article  PubMed  Google Scholar 

  • Culham JC, Danckert SL, DeSouza JF, Gati JS, Menon RS, Goodale MA (2003) Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas. Exp Brain Res 153:180–189

    Article  PubMed  Google Scholar 

  • Culham JC, Cavina-Pratesi C, Singhal A (2006) The role of parietal cortex in visuomotor control: what have we learned from neuroimaging? Neuropsychologia 44:2668–2684

    Article  PubMed  Google Scholar 

  • Damasio H (2005) Human brain anatomy in computerized images. Oxford University Press, Oxford

    Book  Google Scholar 

  • Desmurget M, Epstein CM, Turner RS, Prablanc C, Alexander GE, Grafton ST (1999) Role of the posterior parietal cortex in updating reaching movements to a visual target. Nat Neurosci 2:492–494

    Article  Google Scholar 

  • Duvernoy HM (1999) The human brain. Surface, blood supply, and three-dimensional sectional anatomy. Springer-Verlag, Wien

    Google Scholar 

  • Ellison A, Cowey A (2006) TMS can reveal contrasting functions of the dorsal and ventral visual processing streams. Exp Brain Res 175:618–625

    Article  PubMed  Google Scholar 

  • Fang F, He S (2005) Cortical responses to invisible objects in the human dorsal and ventral pathways. Nat Neurosci 8:1380–1385

    Article  CAS  PubMed  Google Scholar 

  • Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1–47

    Article  CAS  PubMed  Google Scholar 

  • Fuchs M, Kastner J, Wagner M, Hawes S, Ebersole JS (2002) A standardized boundary element method volume conductor model. Clin Neurophysiol 113:702–712

    Article  PubMed  Google Scholar 

  • Fuggetta G, Fiaschi A, Manganotti P (2005) Modulation of cortical oscillatory activities induced by varying single-pulse transcranial magnetic stimulation intensity over the left primary motor area: a combined EEG and TMS study. Neuroimage 27:896–908

    Article  PubMed  Google Scholar 

  • Fuggetta G, Pavone EF, Fiaschi A, Manganotti P (2008) Acute modulation of cortical oscillatory activities during short trains of high-frequency repetitive transcranial magnetic stimulation of the human motor cortex: a combined EEG and TMS study. Hum Brain Mapp 29:1–13

    Article  PubMed  Google Scholar 

  • Goodale MA (2008) Action without perception in human vision. Cogn Neuropsychol 25:891–919

    Article  PubMed  Google Scholar 

  • Grosbras MH, Laird AR, Paus T (2005) Cortical regions involved in eye movements, shifts of attention, and gaze perception. Hum Brain Mapp 25:140–154

    Article  PubMed  Google Scholar 

  • Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey CJ, Wedeen VJ (2008) Mapping the structural core of human cerebral cortex. PLoS Biol 6:1479–1493

    Article  CAS  Google Scholar 

  • Holz EM, Doppelmayr M, Klimesch W, Sauseng P (2008) EEG correlates of action observation in humans. Brain Topogr 21:93–99

    Article  PubMed  Google Scholar 

  • Ilmoniemi RJ, Virtanen J, Ruohonen J, Karhu J, Aronen HJ, Naatanen R, Katila T (1997) Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity. Neuroreport 8:3537–3540

    Article  CAS  PubMed  Google Scholar 

  • Kable JW, Kan IP, Wilson A, Thompson-Schill SL, Chatterjee A (2005) Conceptual representations of action in the lateral temporal cortex. J Cogn Neurosci 17:1855–1870

    Article  PubMed  Google Scholar 

  • Keizer AW, Colzato LS, Hommel B (2008) Integrating faces, houses, motion, and action: spontaneous binding across ventral and dorsal processing streams. Acta Psychol (Amst) 127:177–185

    Article  Google Scholar 

  • Kellenbach ML, Brett M, Patterson K (2003) Actions speak louder than functions: the importance of manipulability and action in tool representation. J Cogn Neurosci 15:30–46

    Article  PubMed  Google Scholar 

  • Komssi S, Kahkonen S (2006) The novelty value of the combined use of electroencephalography and transcranial magnetic stimulation for neuroscience research. Brain Res Rev 52:183–192

    Article  PubMed  Google Scholar 

  • Komssi S, Aronen HJ, Huttunen J, Kesaniemi M, Soinne L, Nikouline VV, Ollikainen M, Roine RO, Karhu J, Savolainen S, Ilmoniemi RJ (2002) Ipsi- and contralateral EEG reactions to transcranial magnetic stimulation. Clin Neurophysiol 113:175–184

    Article  PubMed  Google Scholar 

  • Lee JH, van Donkelaar P (2006) The human dorsal premotor cortex generates on-line error corrections during sensorimotor adaptation. J Neurosci 26:3330–3334

    Article  CAS  PubMed  Google Scholar 

  • Lorenzo-Lopez L, Amenedo E, Pascual-Marqui RD, Cadaveira F (2008) Neural correlates of age-related visual search decline: a combined ERP and sLORETA study. Neuroimage 41:511–524

    Article  PubMed  Google Scholar 

  • MacKay WA, Mendonça AJ (1995) Field potential oscillatory bursts in parietal cortex before and during reach. Brain Res 704:167–174

    Article  CAS  PubMed  Google Scholar 

  • Mahon BZ, Milleville SC, Negri GAL, Rumiati RI, Caramazza A, Martin A (2007) Action-related properties of objects shape object representations in the ventral stream. Neuron 55:507–520

    Article  CAS  PubMed  Google Scholar 

  • Massimini M, Ferrarelli F, Huber R, Esser SK, Singh H, Tononi G (2005) Breakdown of cortical effective connectivity during sleep. Science 309:2228–2232

    Article  CAS  PubMed  Google Scholar 

  • Matelli M, Luppino G (2001) Parietofrontal circuits for action and space perception in the macaque monkey. Neuroimage 14:s27–s32

    Article  CAS  PubMed  Google Scholar 

  • Milner AD, Goodale MA (2006) The visual brain in action. Oxford University Press, Oxford

    Google Scholar 

  • Miniussi C, Thut G (2009) Combining TMS and EEG offers new prospects in cognitive neuroscience. Brain Topogr (in press). doi:10.1007/s10548-009-0083-8

  • Mulert C, Jager L, Schmitt R, Bussfeld P, Pogarell O, Moller HJ, Juckel G, Hegerl U (2004) Integration of fMRI and simultaneous EEG: towards a comprehensive understanding of localization and time-course of brain activity in target detection. Neuroimage 22:83–94

    Article  PubMed  Google Scholar 

  • Nichols TE, Holmes PA (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15:1–25

    Article  PubMed  Google Scholar 

  • Okamoto M, Dan H, Sakamoto K, Takeo K, Shimizu K, Kohno S, Oda I, Isobe S, Suzuki T, Kohyama K, Dan I (2004) Three-dimensional probabilistic anatomical cranio-cerebral correlation via the international 10–20 system oriented for transcranial functional brain mapping. Neuroimage 21:99–111

    Article  PubMed  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  CAS  PubMed  Google Scholar 

  • Oliveri M, Turriziani P, Carlesimo GA, Koch G, Tomaiuolo F, Panella M, Caltagirone C (2001) Parieto-frontal interactions in visual-object and visual-spatial working memory: evidence from transcranial magnetic stimulation. Cereb Cortex 11:606–618

    Article  CAS  PubMed  Google Scholar 

  • Op de Beeck H, Béatse E, Wagemans J, Sunaert S, Van Hecke P (2000) The representation of shape in the context of visual object categorization tasks. Neuroimage 12:28–40

    Article  CAS  PubMed  Google Scholar 

  • Pascual-Marqui RD (2002) Standardized low resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol 24D:5–12

    Google Scholar 

  • Pascual-Marqui RD, Michel CM, Lehmann D (1994) Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain. Int J. Psychophysiol 18:49–65

    Article  CAS  PubMed  Google Scholar 

  • Pascual-Marqui RD, Esslen M, Kochi K, Lehmann D (2002) Functional imaging with low-resolution brain electromagnetic tomography (LORETA): a review. Methods Find Exp Clin Pharmacol 24(Suppl C):91–95

    PubMed  Google Scholar 

  • Praeg E, Esslen M, Lutz K, Jancke L (2006) Neuronal modifications during visuomotor association learning assessed by electric brain tomography. Brain Topogr 19:61–75

    Article  PubMed  Google Scholar 

  • Rizzolatti G, Fogassi L, Gallese V (1997) Parietal cortex: from sight to action. Curr Opin Neurobiol 7:562–567

    Article  CAS  PubMed  Google Scholar 

  • Rossini PM, Barker AT, Berardelli A, Caramia MD, Caruso G, Cracco RG, Dimitrijevic MR, Hallett M, Katayama Y, Lucking CH, Maertens de Nordhout AL, Marsden CD, Murray NMF, Rothwell JC, Swash M, Tomberg C (1994) Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol 91:79–92

    Article  CAS  PubMed  Google Scholar 

  • Rushworth MF, Johansen-Berg H, Göbel SM, Devlin JT (2003) The left parietal and premotor cortices: motor attention and selection. Neuroimage 20:S89–S100

    Article  PubMed  Google Scholar 

  • Ryan S, Bonilha L, Jackson SR (2006) Individual variation in the location of the parietal eye fields: a TMS study. Exp Brain Res 173:389–394

    Article  PubMed  Google Scholar 

  • Sack AT, Linden DE (2003) Combining transcranial magnetic stimulation and functional imaging in cognitive brain research: possibilities and limitations. Brain Res Brain Res Rev 43:41–56

    Article  PubMed  Google Scholar 

  • Schenk T, Milner AD (2006) Concurrent visuomotor behaviour improves form discrimination in a patient with visual form agnosia. Eur J Neurosci 24:1495–1503

    Article  PubMed  Google Scholar 

  • Schutter DJ, van Honk J (2006) An electrophysiological link between the cerebellum, cognition and emotion: frontal theta EEG activity to single-pulse cerebellar TMS. Neuroimage 33:1227–1231

    Article  PubMed  Google Scholar 

  • Sekihara K, Sahani M, Nagarajan SS (2005) Localization bias and spatial resolution of adaptive and non-adaptive spatial filters for MEG source reconstruction. Neuroimage 25:1056–1067

    Article  PubMed  Google Scholar 

  • Shmuelof L, Zohary E (2005) Dissociation between ventral and dorsal fMRI activation during object action recognition. Neuron 47:457–470

    Article  CAS  PubMed  Google Scholar 

  • Silvanto J, Pascual-Leone A (2008) State-dependency of transcranial magnetic stimulation. Brain Topogr 21:1–10

    Article  PubMed  Google Scholar 

  • Slagter HA, Giesbrecht B, Kok A, Weissman DH, Kenemans JL, Woldorff MG, Mangun GR (2007) fMRI evidence for both generalized and specialized components of attentional control. Brain Res 1177:90–102

    Article  CAS  PubMed  Google Scholar 

  • Talairach J, Tournoux P (1988) Co-Planar stereotaxic atlas of the human brain: three dimensional proprtional system. Georg Thieme, Stuttgart

    Google Scholar 

  • Tannè-Gariepy J, Rouiller EM, Boussaud D (2002) Parietal inputs to dorsal versus ventral premotor areas in the macaque monkey: evidence for largely segregated visuomotor pathways. Exp Brain Res 145:91–103

    Article  PubMed  Google Scholar 

  • Taylor PC, Walsh V, Eimer M (2008) Combining TMS and EEG to study cognitive function and cortico-cortico interactions. Behav Brain Res 191:141–147

    Article  PubMed  Google Scholar 

  • Thayer ZC, Johnson BW (2006) Cerebral processes during visuo-motor imagery of hands. Psychophysiology 43:401–412

    Article  PubMed  Google Scholar 

  • Thomsen T, Specht K, Ersland L, Hugdahl K (2005) Processing of conflicting cues in an attention-shift paradigm studied with fMRI. Neurosci Lett 380:138–142

    Article  CAS  PubMed  Google Scholar 

  • Thuraisingham RA, Tran Y, Boord P, Craig A (2007) Analysis of eyes open, eye closed EEG signals using second-order difference plot. Med Biol Eng Comput 45:1243–1249

    Article  PubMed  Google Scholar 

  • Thut G, Miniussi C (2009) New insights into rhythmic brain activity from TMS-EEG studies. Trends Cogn Sci 13:182–189

    Article  PubMed  Google Scholar 

  • Valyear KF, Culham JC, Sharif N, Westwood D, Goodale MA (2006) A double dissociation between sensitivity to changes in object identity and object orientation in the ventral and dorsal visual streams: a human fMRI study. Neuropsychologia 44:218–228

    Article  PubMed  Google Scholar 

  • Van Donkelaar P, Lee JH, Drew AS (2000) Transcranial magnetic stimulation disrupts eye-hand interactions in the posterior parietal cortex. J Neurophysiol 84:1677–1680

    PubMed  Google Scholar 

  • Van Donkelaar P, Lee JH, Drew AS (2002) Eye-hand interactions differ in the human premotor and parietal cortices. Hum Mov Sci 21:377–386

    PubMed  Google Scholar 

  • Vitacco D, Brandeis D, Pascual-Marqui RD, Martin E (2002) Correspondence of event-related potential tomography and functional magnetic resonance imaging during language processing. Hum Brain Mapp 17:4–12

    Article  PubMed  Google Scholar 

  • Walsh V, Pascual-Leone A (2003) A neurochronometrics of mind. The MIT Press, Cambridge, Massachusetts

    Google Scholar 

  • Wassermann EM (1998) Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Stimulation, June 5–7, 1996. Electroencephalogr Clin Neurophysiol 108:1–16

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from Ministero dell’Università e della Ricerca, Italy. Authors also wish to thank the anonymous Reviewers for useful suggestions which strongly improved the readability of the manuscript.

Author information

Authors and Affiliations

  1. BRAIN Center for Neuroscience, Department of Life Sciences, University of Trieste, Via Fleming, 22, 34127, Trieste, Italy

    Marco Zanon, Pierpaolo Busan & Piero Paolo Battaglini

  2. Department of Clinical and Experimental Medicine and Clinical and Experimental Neuroscience, University of Trieste, Trieste, Italy

    Fabrizio Monti & Gilberto Pizzolato

Authors
  1. Marco Zanon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pierpaolo Busan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fabrizio Monti
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gilberto Pizzolato
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Piero Paolo Battaglini
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pierpaolo Busan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zanon, M., Busan, P., Monti, F. et al. Cortical Connections Between Dorsal and Ventral Visual Streams in Humans: Evidence by TMS/EEG Co-Registration. Brain Topogr 22, 307–317 (2010). https://doi.org/10.1007/s10548-009-0103-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10548-009-0103-8

Keywords

Search

Navigation