Abstract
In this chapter we describe a novel approach which enhances the functional resolution of transcranial magnetic stimulation (TMS) to a level that allows for differential stimulation of functionally distinct neuronal populations within a cortical area. It is based on the well-known principle of state-dependency: a phenomenon whereby the response of a system to an external stimulus is affected not only by the properties of that stimulus but also by the internal state of the system. With regard to TMS, the neural impact of an applied pulse is determined not only by the stimulation parameters but also by the initial activation state of the affected neurons; therefore, neurons within a cortical area will be differentially affected by TMS if their initial activation states at the time of stimulation are dissimilar. The basic idea in state-dependent TMS is to control this initial state/TMS interaction. By selectively increasing the susceptibility of a specific neuronal population via adaptation and priming, one can differentially stimulate this population from other neurons in the area. The main benefit of state-dependent TMS is that it allows TMS research to move beyond questions of βIs region X necessary for task Yβ and investigate the functional neuronal properties within a targeted area. So far, this approach has been successfully used to investigate neuronal representations associated with a wide range of cognitive functions such as numerical cognition, action observation, and conceptual knowledge, and it may hold much promise for future research.
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References
Silvanto J, Pascual-Leone A (2008) State-dependency of transcranial magnetic stimulation. Brain Topogr 21:1β10
Zeki S, Watson JD, Lueck CJ, Friston KJ, Kennard C, Frackowiak RS (1991) A direct demonstration of functional specialization in human visual cortex. J Neurosci 11:641β649
Lamme VA, SupΓ¨r H, Landman R, Roelfsema PR, Spekreijse H (2000) The role of primary visual cortex (V1) in visual awareness. Vision Res 40:1507β1521
Maunsell JH, Van Essen DC (1983) Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. J Neurophysiol 49:1127β1147
Malach R, Reppas J, Benson R, Kwong K, Jiang H, Kennedy W, Ledden P, Brady T, Rosen B, Tootell R (1995) Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. Proc Natl Acad Sci U S A 92:8135β8139
Grill-Spector K, Kourtzi Z, Kanwisher N (2001) The lateral occipital complex and its role in object recognition. Vision Res 41(10β11):1409β1422
Rolls ET (2000) Functions of the primate temporal lobe cortical visual areas in invariant visual object and face recognition. Neuron 27:205β218
Walsh V, Pascual-Leone A (2003) Transcranial magnetic stimulation: a neurochronometrics of mind. MIT Press, Cambridge
Amassian VE, Cracco RQ, Maccabee PJ, Cracco JB, Rudell A, Eberle L (1989) Suppression of visual perception by magnetic coil stimulation of human occipital cortex. Electroencephalogr Clin Neurophysiol 74:458β462
Silvanto J, Cowey A, Lavie N, Walsh V (2005) Striate cortex V1 activity gates awareness of motion. Nat Neurosci 8:143β144
Grill-Spector K, Henson R, Martin A (2006) Repetition and the brain: neural models of stimulus-specific effects. Trends Cogn Sci 10:14β23
Gibson J, Radner M (1937) Adaptation, after-effect and contrast in the perception of tilted lines. J Exp Psychol 12:453β467
Mather G, Verstraten F, Anstis S (1998) The motion aftereffect: a modern perspective. Oxford University Press, Oxford
Grill-Spector K, Kushnir T, Edelman S, Avidan G, Itzchak Y, Malach R (1999) Differential processing of objects under various viewing conditions in the human lateral occipital complex. Neuron 24:187β203
Grill-Spector K, Malach R (2001) fMR-adaptation: a tool for studying the functional properties of human cortical neurons. Acta Psychol 107:293β321
Silvanto J, Muggleton NG (2008) New light through old windows: moving beyond the βvirtual lesionβ approach to transcranial magnetic stimulation. Neuroimage 39:549β552
Siebner HR, Lang N, Rizzo V, Nitsche MA, Paulus W, Lemon RN et al (2004) Preconditioning of low-frequency repetitive transcranial magnetic stimulation with transcranial direct current stimulation: evidence for homeostatic plasticity in the human motor cortex. J Neurosci 24:3379β3385
Silvanto J, Cattaneo Z, Battelli L, Pascual-Leone A (2008) Baseline cortical excitability determines whether TMS disrupts or facilitates behavior. J Neurophysiol 99:2725β2730
Silvanto J, Muggleton NG, Cowey A, Walsh V (2007) Neural adaptation reveals state-dependent effects of transcranial magnetic stimulation. Eur J Neurosci 25:1874β1881
Engel SA (2005) Adaptation of oriented and unoriented color-selective neurons in human visual areas. Neuron 45:613β623
Cattaneo Z, Silvanto J (2008) Investigating visual motion perception using the TMS-adaptation paradigm. Neuroreport 19:1423β1427
Cattaneo Z, Silvanto J (2008) Time course of the state-dependent effect of transcranial magnetic stimulation motion in the TMS-adaptation paradigm. Neurosci Lett 443: 82β85
Cattaneo Z, Devlin JT, Vecchi T, Silvanto J (2009) Dissociable neural representations of grammatical gender in Brocaβs area investigated by the combination of satiation and TMS. Neuroimage 47:700β704
Smith L, Klein R (1990) Evidence for semantic satiation: repeating a category slows subsequent semantic processing. J Exp Psychol Learn Mem Cogn 16:852β861
Smith LC (1984) Semantic satiation affects category membership decision time but not lexical priming. Mem Cogn 12:483β488
ThΓ©oret H, Kobayashi M, Ganis G, Di Capua P, Pascual-Leone A (2002) Repetitive transcranial magnetic stimulation of human area MT/V5 disrupts storage of the motion aftereffect. Neuropsychologia 40:2280β2287
Cattaneo Z, Devlin JT, Salvini F, Vecchi T, Silvanto J (2010) The causal role of category-specific neuronal representations in the left ventral premotor cortex (PMv) in semantic processing. Neuroimage 49:2728β2734
Cohen Kadosh R, Muggleton N, Silvanto J, Walsh V (2010) Double dissociation of format-dependent and number-specific neurons in human parietal cortex. Cereb Cortex 209:2166β2171
Maljkovic V, Nakayama K (1994) Priming of pop-out: I. Role of features. Mem Cognit 22:657β672
Maljkovic V, Nakayama K (1996) Priming of pop-out: II. The role of position. Percept Psychophys 58:977β991
Campana G, Cowey A, Walsh V (2002) Priming of motion direction and area V5/MT: a test of perceptual memory. Cereb Cortex 12:663β669
Magnussen S, Greenlee MW (1999) The psychophysics of perceptual memory. Psychol Res 62:81β92
Cattaneo Z, Rota F, Walsh V, Vecchi T, Silvanto J (2009) TMS-adaptation reveals abstract letter selectivity in the left posterior parietal cortex (PPC). Cereb Cortex 19:2321β2325
Cattaneo L, Sandrini M, Schwarzbach J (2010) State-dependent TMS reveals a hierarchical representation of observed acts in the temporal, parietal, and premotor cortices. Cereb Cortex 209:2252β2258
Silvanto J, Schwarzkopf DS, Gilaie-Dotan S, Rees G (2010) Differing causal roles for lateral occipital cortex and occipital face area in invariant shape recognition. Eur J Neurosci 32:165β171
Mattavelli G, Cattaneo Z, Papagno C (2011) Transcranial magnetic stimulation of medial prefrontal cortex modulates face expressions processing in a priming task. Neuropsychologia 49(5):992β998
Pavan A, Campana G, Maniglia M, Casco C (2010) The role of high-level visual areas in short- and longer-lasting forms of neural plasticity. Neuropsychologia 48:3069β3079
Voss JL, Schendan HE, Paller KA (2010) Finding meaning in novel geometric shapes influences electrophysiological correlates of repetition and dissociates perceptual and conceptual priming. Neuroimage 49:2879β2889
Miniussi C, Ruzzoli M, Walsh V (2010) The mechanism of transcranial magnetic stimulation in cognition. Cortex 46(1):128β130
Kitajo K, Nozaki D, Ward LM, Yamamoto Y (2003) Behavioral stochastic resonance within the human brain. Phys Rev Lett 90:218103
Lugo E, Doti R, Faubert J (2008) Ubiquitous crossmodal Stochastic Resonance in humans: auditory noise facilitates tactile, visual and proprioceptive sensations. PLoS ONE 3:e2860
Sasaki H, Sakane S, Ishida T, Todorokihara M, Kitamura T, Aoki R (2008) Suprathreshold stochastic resonance in visual signal detection. Behav Brain Res 193:152β155
Simonotto E, Riani M, Seife C, Roberts M, Twitty J, Moss F (1997) Visual perception of stochastic resonance. Phys Rev Lett 78:1186
Schwarzkopf DS, Silvanto J, Rees G (2011) Stochastic resonance effects reveal the neural mechanisms of transcranial magnetic stimulation. J Neurosci 31(9):3143β3147
Ruzzoli M, Marzi CA, Miniussi C (2010) The neural mechanisms of the effects of transcranial magnetic stimulation on perception. J Neurophysiol 103(6):2982β2989
Ruzzoli M, Abrahamyan A, Clifford CW, Marzi CA, Miniussi C, Harris JA (2011) The effect of TMS on visual motion sensitivity: an increase in neural noise or a decrease in signal strength? J Neurophysiol (1):138β143
Gilaie-Dotan S, Nir Y, Malach R (2008) Regionally-specific adaptation dynamics in human object areas. Neuroimage 39:1926β1937
Adolphs R, Damasio H, Tranel D, Cooper G, Damasio AR (2000) A role for somatosensory cortices in the visual recognition of emotion as revealed by three-dimensional lesion mapping. J Neurosci 20:2683β2690
Heberlein AS, Padon AA, Gillihan SJ, Farah MJ, Fellows LK (2008) Ventromedial frontal lobe plays a critical role in facial emotion recognition. J Cogn Neurosci 20:721β733
Mah LWY, Arnold MC, Grafman J (2005) Deficits in social knowledge following damage to ventromedial prefrontal cortex. J Neuro-psychiatry Clin Neurosci 17:66β74
Pitcher D, Garrido L, Walsh V, Duchaine C (2008) Transcranial Magnetic Stimulation disrupts the perception and embodiment of facial expression. J Neurosci 28:8929β8933
Piazza M, Pinel P, Le Bihan D, Dehaene S (2007) A magnitude code common to numerosities and number symbols in human intraparietal cortex. Neuron 53:293β305
Dehaene S, Dehaene-Lambertz G, Cohen L (1998) Abstract representations of numbers in the animal and human brain. Trends Neurosci 21:355β361
Grafton ST, Hamilton AF (2007) Evidence for a distributed hierarchy of action representation in the brain. Hum Motor Sci 26:590β616
Cattaneo L, Rizzolatti G (2009) The mirror neuron system. Arch Neurol 66:557β560
Chao LL, Haxby JV, Martin A (1999) Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects. Nat Neurosci 2:913β919
Devlin JT, Rushworth MF, Matthews PM (2005) Category-related activation for written words in the posterior fusiform is task specific. Neuropsychologia 43:69β74
Damasio H, Grabowski TJ, Tranel D, Hichwa RD, Damasio AR (1996) A neural basis for lexical retrieval. Nature 380:499β505
Martin A, Wiggs CL, Ungerleider LG, Haxby JV (1996) Neural correlates of category specific knowledge. Nature 379:649β652
Baddeley A, Salame P (1986) The unattended speech effect: perception or memory? J Exp Psychol Learn Mem Cogn 12:525β529
Cornoldi C, Vecchi T (2003) Visuo-spatial working memory and individual differences. Psychology Press, Hove
Cattaneo Z, Vecchi T, Pascual-Leone A, Silvanto J (2009) Contrasting early visual cortical activation states causally involved in visual imagery and short-term memory. Eur J Neurosci 30(7):1393β1400
Sparing R, Mottaghy FM, Ganis G, Thompson WL, TΓΆpper R, Kosslyn SM, Pascual-Leone A (2002) Visual cortex excitability increases during visual mental imageryβa TMS study in healthy human subjects. Brain Res 938:s92β97
Kosslyn SM, Ganis G, Thompson WL (2001) Neural foundations of imagery. Nat Rev Neurosci 2:635β642
Sack AT, Jacobs C, De Martino F, Staeren N, Goebel R, Formisano E (2008) Dynamic premotor-to-parietal interactions during spatial imagery. J Neurosci 28:8417β8429
Sack AT, Sperling JM, Prvulovic D, Formisano E, Goebel R, Di Salle F, Dierks T, Linden DE (2002) Tracking the mindβs image in the brain II: transcranial magnetic stimulation reveals parietal asymmetry in visuospatial imagery. Neuron 35:195β204
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Silvanto, J., Cattaneo, Z. (2014). State-Dependent Transcranial Magnetic Stimulation (TMS) Protocols. In: Rotenberg, A., Horvath, J., Pascual-Leone, A. (eds) Transcranial Magnetic Stimulation. Neuromethods, vol 89. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-0879-0_9
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DOI: https://doi.org/10.1007/978-1-4939-0879-0_9
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