The effect of unpredicted visual feedback on activation in the secondary somatosensory cortex during movement execution

BMC Neuroscience

Ryusuke Kakigi¹  Toshiaki Wasaka¹ 

[1] Department of Integrative Physiology, National Institute for Physiological Sciences, 38 Nishigonaka, Myodaiji, Okazaki, Aichi, 4448585, Japan

关键词: SII;    Bimanual movement;    Sensorimotor integration;    MEG;   

Others  :  1140795
DOI  :  10.1186/1471-2202-13-138

 received in 2012-06-14, accepted in 2012-10-25,  发布年份 2012

【 摘 要 】

Background

A mechanism that monitors the congruence between sensory inputs and motor outputs is necessary to control voluntary movement. The representation of limb position is constantly updated on the basis of somatosensory and visual information and efference copy from motor areas. However, the cortical mechanism underlying detection of limb position using somatosensory and visual information has not been elucidated. This study investigated the influence of visual feedback on information processing in somatosensory areas during movement execution using magnetoencephalography. We used an experimental condition in which the visual information was incongruent despite the motor execution and somatosensory feedback being congruent. Subjects performed self-paced bimanual movements of both thumbs, either symmetric or asymmetric, under normal visual and mirrored conditions. The mirror condition provided a visual feedback by showing a reflection of the subject’s right hand in place of the left hand. Therefore, in the Asymmetric task of the Mirror condition, subjects saw symmetric movements despite performing asymmetric movements.

Results

Activation in the primary somatosensory area (SI) revealed inhibition of neural activity and that in the secondary somatosensory area (SII) showed enhancement with voluntary movement. In addition, the SII contralateral to the side of stimulation was significantly enhanced in the Asymmetric task of the Mirror condition, which provided non-veridical visual feedback.

Conclusions

These results suggested that visual information influenced the neuronal activity concerning sensorimotor interaction in the SII during motor execution. The SII contributes to the detection of unpredicted visual feedback of movement execution.

【 授权许可】

   
2012 Wasaka and Kakigi; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】

• [1]Shadmehr R, Krakauer JW: A computational neuroanatomy for motor control. Exp Brain Res 2008, 185:359-381.
• [2]Wolpert DM, Miall RC, Kawato M: Internal models in the cerebellum. Trends Cogn Sci 1998, 2:338-347.
• [3]Kida T, Inui K, Wasaka T, Akatsuka K, Tanaka E, Kakigi R: Time-varying cortical activations related to visual-tactile cross-modal links in spatial selective attention. J Neurophysiol 2007, 97:3585-3596.
• [4]Macaluso E, Frith CD, Driver J: Modulation of human visual cortex by crossmodal spatial attention. Science 2000, 289:1206-1208.
• [5]Schurmann M, Kolev V, Menzel K, Yordanova J: Spatial coincidence modulates interaction between visual and somatosensory evoked potentials. Neuroreport 2002, 13:779-783.
• [6]vanBeers RJ, Sittig AC, vanderGon JJD: How humans combine simultaneous proprioceptive and visual position information. Exp Brain Res 1996, 111:253-261.
• [7]Botvinick M, Cohen J: Rubber hands ‘feel’ touch that eyes see. Nature 1998, 391:756.
• [8]Graziano MSA: Where is my arm? The relative role of vision and proprioception in the neuronal representation of limb position. P Natl Acad Sci USA 1999, 96:10418-10421.
• [9]MonWilliams M, Wann JP, Jenkinson M, Rushton K: Synaesthesia in the normal limb. P Roy Soc B-Biol Sci 1997, 264:1007-1010.
• [10]Cardini F, Longo MR, Haggard P: Vision of the body modulates somatosensory intracortical inhibition. Cereb Cortex 2011, 21:2014-2022.
• [11]Kennett S, Spence C, Driver J: Visuo-tactile links in covert exogenous spatial attention remap across changes in unseen hand posture. Percept Psychophys 2002, 64:1083-1094.
• [12]Taylor-Clarke M, Kennett S, Haggard P: Vision modulates somatosensory cortical processing. Curr Biol 2002, 12:233-236.
• [13]Eimer M, Forster B, Fieger A, Harbich S: Effects of hand posture on preparatory control processes and sensory modulations in tactile-spatial attention. Clin Neurophysiol 2004, 115:596-608.
• [14]Sambo CF, Gillmeister H, Forster B: Viewing the body modulates neural mechanisms underlying sustained spatial attention in touch. Eur J Neurosci 2009, 30:143-150.
• [15]Avikainen S, Forss N, Hari R: Modulated activation of the human SI and SII cortices during observation of hand actions. NeuroImage 2002, 15:640-646.
• [16]Mottonen R, Jarvelainen J, Sams M, Hari R: Viewing speech modulates activity in the left SI mouth cortex. NeuroImage 2005, 24:731-737.
• [17]Pihko E, Nangini C, Jousmaki V, Hari R: Observing touch activates human primary somatosensory cortex. Eur J Neurosci 2010, 31:1836-1843.
• [18]Rossi S, Tecchio F, Pasqualetti P, Ulivelli M, Pizzella V, Romani GL, Passero S, Battistini N, Rossini PM: Somatosensory processing during movement observation in humans. Clin Neurophysiol 2002, 113:16-24.
• [19]Wasaka T, Kakigi R: Conflict caused by visual feedback modulates activation in somatosensory areas during movement execution. NeuroImage 2012, 59:1501-1507.
• [20]Altschuler EL, Wisdom SB, Stone L, Foster C, Galasko D, Llewellyn DM, Ramachandran VS: Rehabilitation of hemiparesis after stroke with a mirror. Lancet 1999, 353:2035-2036.
• [21]Ramachandran VS, Rogers-Ramachandran D: Synaesthesia in phantom limbs induced with mirrors. Proc Biol Sci 1996, 263:377-386.
• [22]Ramachandran VS, Rogers-Ramachandran D, Cobb S: Touching the phantom limb. Nature 1995, 377:489-490.
• [23]Oldfield RC: The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
• [24]Kida T, Wasaka T, Inui K, Akatsuka K, Nakata H, Kakigi R: Centrifugal regulation of human cortical responses to a task-relevant somatosensory signal triggering voluntary movement. NeuroImage 2006, 32:1355-1364.
• [25]Hamalainen M, Hari R, Ilmoniemi R, Kunuutila J, Lounasmaa OV: Magnetoencephalography-Theory, instrumentation, and application to noninvasive studies of the working human brain. Rev Mod Phys 1993, 65:413-497.
• [26]Tipper SP, Lloyd D, Shorland B, Dancer C, Howard LA, McGlone F: Vision influences tactile perception without proprioceptive orienting. Neuroreport 1998, 9:1741-1744.
• [27]Kennett S, Taylor-Clarke M, Haggard P: Noninformative vision improves the spatial resolution of touch in humans. Curr Biol 2001, 11:1188-1191.
• [28]Longo MR, Pernigo S, Haggard P: Vision of the body modulates processing in primary somatosensory cortex. Neurosci Lett 2011, 489:159-163.
• [29]Kakigi R, Koyama S, Hoshiyama M, Watanabe S, Shimojo M, Kitamura Y: Gating of somatosensory evoked responses during active finger movements magnetoencephalographic studies. J Neurol Sci 1995, 128:195-204.
• [30]Kakigi R, Shimojo M, Hoshiyama M, Koyama S, Watanabe S, Naka D, Suzuki H, Nakamura A: Effects of movement and movement imagery on somatosensory evoked magnetic fields following posterior tibial nerve stimulation. Brain Res Cogn Brain Res 1997, 5:241-253.
• [31]Rushton DN, Rothwell JC, Craggs MD: Gating of somatosensory evoked potentials during different kinds of movement in man. Brain 1981, 104:465-491.
• [32]Wasaka T, Hoshiyama M, Nakata H, Nishihira Y, Kakigi R: Gating of somatosensory evoked magnetic fields during the preparatory period of self-initiated finger movement. NeuroImage 2003, 20:1830-1838.
• [33]Wasaka T, Kida T, Nakata H, Akatsuka K, Kakigi R: Characteristics of sensori-motor interaction in the primary and secondary somatosensory cortices in humans: a magnetoencephalography study. Neuroscience 2007, 149:446-456.
• [34]Wasaka T, Nakata H, Akatsuka K, Kida T, Inui K, Kakigi R: Differential modulation in human primary and secondary somatosensory cortices during the preparatory period of self-initiated finger movement. Eur J Neurosci 2005, 22:1239-1247.
• [35]Desmurget M, Grafton S: Forward modeling allows feedback control for fast reaching movements. Trends Cogn Sci 2000, 4:423-431.
• [36]von Holst E, Mittelstaedt H: Das Reafferenzprinzip: Wechselwirkungen Zwischen Zentralnervensystem und Peripherie. Natursissenschaften 1950, 37:464-476.
• [37]Sperry RW: Neural basis of the spontaneous optokinetic response produced by visual inversion. J Comp Physiol Psychol 1950, 43:482-489.
• [38]Blakemore SJ, Goodbody SJ, Wolpert DM: Predicting the consequences of our own actions: the role of sensorimotor context estimation. J Neurosci 1998, 18:7511-7518.
• [39]Blakemore SJ, Wolpert DM, Frith CD: Central cancellation of self-produced tickle sensation. Nat Neurosci 1998, 1:635-640.
• [40]Hesse MD, Nishitani N, Fink GR, Jousmaki V, Hari R: Attenuation of somatosensory responses to self-produced tactile stimulation. Cereb Cortex 2010, 20:425-432.
• [41]Miall RC, Christensen LO, Cain O, Stanley J: Disruption of state estimation in the human lateral cerebellum. PLoS Biol 2007, 5:e316.
• [42]Fourneret P, Jeannerod M: Limited conscious monitoring of motor performance in normal subjects. Neuropsychologia 1998, 36:1133-1140.
• [43]Farrer C, Frey SH, Van Horn JD, Tunik E, Turk D, Inati S, Grafton ST: The angular gyrus computes action awareness representations. Cereb Cortex 2008, 18:254-261.
• [44]Farrer C, Franck N, Georgieff N, Frith CD, Decety J, Jeannerod M: Modulating the experience of agency: a positron emission tomography study. NeuroImage 2003, 18:324-333.
• [45]Farrer C, Frith CD: Experiencing oneself vs another person as being the cause of an action: the neural correlates of the experience of agency. NeuroImage 2002, 15:596-603.
• [46]Karnath HO, Baier B: Right insula for our sense of limb ownership and self-awareness of actions. Brain Struct Funct 2010, 214:411-417.
• [47]Karnath HO, Baier B, Nagele T: Awareness of the functioning of one’s own limbs mediated by the insular cortex? J Neurosci 2005, 25:7134-7138.
• [48]Inui K, Wang X, Qiu Y, Nguyen BT, Ojima S, Tamura Y, Nakata H, Wasaka T, Tran TD, Kakigi R: Pain processing within the primary somatosensory cortex in humans. Eur J Neurosci 2003, 18:2859-2866.