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Erschienen in: Experimental Brain Research 1/2004

01.01.2004 | Research Article

Tactile stimulus predictability modulates activity in a tactile-motor cortical network

verfasst von: A. J. Nelson, W. R. Staines, W. E. McIlroy

Erschienen in: Experimental Brain Research | Ausgabe 1/2004

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Abstract

Manipulating objects in the hand requires the continuous transformation of sensory input into appropriate motor behaviour. Using a novel vibrotactile device combined with fMRI, the cortical network associated with tactile sensorimotor transformations was investigated. Continuous tactile stimuli were delivered in a random or predictable pattern to the second digit on the right hand of all subjects. To better distinguish sensory and motor processes, subjects were instructed to make proportionate motor gripping responses with their left hand. A consistent cortical network of activation was revealed that included the supplementary motor, dorsal and ventral premotor, posterior parietal, primary and secondary somatosensory and primary motor cortex. Tracking the unpredictable versus predictable tactile stimulus led to greater delays in motor responses and to increased performance errors. Cortical effects due to stimulus predictability were observed in several components of the network, though it was most evident as increased cortical activation in frontal motor regions during tracking of unpredictable tactile stimuli. In contrast to the proposed hypotheses, primary and secondary somatosensory cortices contralateral to tactile input did not reveal enhanced responses during unpredictable tracking. Facilitation during unpredictable tracking was also observed in primary somatosensory cortex contralateral to motor responses, the receptive site for movement-related afference. The present study provides a novel and controlled approach to investigate the loci associated with tactile-motor processing and to measure the task-specific effect of stimulus predictability on network components.
Literatur
Zurück zum Zitat Bandettini PA, Jesmanowicz A, Wong EC, Hyde JS (1993) Processing strategies for time-course data sets in functional MRI of the human brain. Mag Res Med 30:161–173 Bandettini PA, Jesmanowicz A, Wong EC, Hyde JS (1993) Processing strategies for time-course data sets in functional MRI of the human brain. Mag Res Med 30:161–173
Zurück zum Zitat Burton H (2002) Cerebral cortical regions devoted to the somatosensory system: results from brain imaging studies in humans. In: Nelson RJ (ed) The somatosensory system: deciphering the brain’s own body image. CRC Press, Boca Raton, FL, pp 27–72 Burton H (2002) Cerebral cortical regions devoted to the somatosensory system: results from brain imaging studies in humans. In: Nelson RJ (ed) The somatosensory system: deciphering the brain’s own body image. CRC Press, Boca Raton, FL, pp 27–72
Zurück zum Zitat Burton H, Sinclair RJ (2000) Attending to and remembering tactile stimuli: a review of brain imaging data and single-neuron responses. J Clin Neurophysiol 17(6):575–591PubMed Burton H, Sinclair RJ (2000) Attending to and remembering tactile stimuli: a review of brain imaging data and single-neuron responses. J Clin Neurophysiol 17(6):575–591PubMed
Zurück zum Zitat Burton H, Abend NS, MacLeod AM, Sinclair RJ, Snyder AZ, Raichle ME (1999) Tactile attention tasks enhance activation in somatosensory regions of parietal cortex: a positron emission tomography study. Cereb Cortex 9:662–74PubMed Burton H, Abend NS, MacLeod AM, Sinclair RJ, Snyder AZ, Raichle ME (1999) Tactile attention tasks enhance activation in somatosensory regions of parietal cortex: a positron emission tomography study. Cereb Cortex 9:662–74PubMed
Zurück zum Zitat Cohen LG, Bandinelli S, Sato S, Kufta C, Hallet M (1991) Attenuation in detection for somatosensory stimuli by transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol 81:366–376CrossRefPubMed Cohen LG, Bandinelli S, Sato S, Kufta C, Hallet M (1991) Attenuation in detection for somatosensory stimuli by transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol 81:366–376CrossRefPubMed
Zurück zum Zitat Cox RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comp Biomed Res 29:162–173CrossRef Cox RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comp Biomed Res 29:162–173CrossRef
Zurück zum Zitat Cox RW, Jesmanowicz A (1999) Real-time 3D image registration for functional MRI. Mag Res Med 42:1014–1018CrossRef Cox RW, Jesmanowicz A (1999) Real-time 3D image registration for functional MRI. Mag Res Med 42:1014–1018CrossRef
Zurück zum Zitat Dassonville P, Lewis SM, Zhu XH, Ugurbil K, Kim SG, Ashe J (1998) Effects of movement predictability on cortical motor activation. Neurosci Res 32(1):65–74CrossRefPubMed Dassonville P, Lewis SM, Zhu XH, Ugurbil K, Kim SG, Ashe J (1998) Effects of movement predictability on cortical motor activation. Neurosci Res 32(1):65–74CrossRefPubMed
Zurück zum Zitat Deiber MP, Passingham RE, Colebatch JG, Friston KJ, Nixon PD, Frackowiak RS (1991) Cortical areas and the selection of movement: a study with positron emission tomography. Exp Brain Res 84:393–402PubMed Deiber MP, Passingham RE, Colebatch JG, Friston KJ, Nixon PD, Frackowiak RS (1991) Cortical areas and the selection of movement: a study with positron emission tomography. Exp Brain Res 84:393–402PubMed
Zurück zum Zitat Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC (1995) Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Mag Res Med 33:636–647 Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC (1995) Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Mag Res Med 33:636–647
Zurück zum Zitat Francis ST, Kelly EF, Bowtell R Dunseath WJ, Folger SE, McGlone F (2000) FMRI of the responses to vibratory stimulation of digit tips. Neuroimage 11:188–202CrossRefPubMed Francis ST, Kelly EF, Bowtell R Dunseath WJ, Folger SE, McGlone F (2000) FMRI of the responses to vibratory stimulation of digit tips. Neuroimage 11:188–202CrossRefPubMed
Zurück zum Zitat Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, Dolan RJ (1997) Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 6:218–29CrossRefPubMed Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, Dolan RJ (1997) Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 6:218–29CrossRefPubMed
Zurück zum Zitat Glover GH, Lai S (1998) Self-navigated spiral fMRI: interleaved versus single-shot. Mag Res Med 39:361–368 Glover GH, Lai S (1998) Self-navigated spiral fMRI: interleaved versus single-shot. Mag Res Med 39:361–368
Zurück zum Zitat Grafton ST, Mazziotta JC, Woods RP, Phelps ME (1992) Human functional anatomy of visually guided finger movements. Brain 115:565–87PubMed Grafton ST, Mazziotta JC, Woods RP, Phelps ME (1992) Human functional anatomy of visually guided finger movements. Brain 115:565–87PubMed
Zurück zum Zitat Graham SJ, Staines WR, Nelson AJ, Plewes DB, McIlroy WE (2001) New devices to deliver somatosensory stimuli during functional magnetic resonance imaging. Mag Res Med 46:436–42CrossRef Graham SJ, Staines WR, Nelson AJ, Plewes DB, McIlroy WE (2001) New devices to deliver somatosensory stimuli during functional magnetic resonance imaging. Mag Res Med 46:436–42CrossRef
Zurück zum Zitat Guillery RW, Feig SL, Lozsadi DA (1998) Paying attention to the thalamic reticular nucleus. Trends Neurosci 21:28–32PubMed Guillery RW, Feig SL, Lozsadi DA (1998) Paying attention to the thalamic reticular nucleus. Trends Neurosci 21:28–32PubMed
Zurück zum Zitat Hansson T, Brismar T (1999) Tactile stimulation of the hand causes bilateral cortical activation: a functional magnetic resonance study in humans. Neurosci Lett 271:29–32CrossRefPubMed Hansson T, Brismar T (1999) Tactile stimulation of the hand causes bilateral cortical activation: a functional magnetic resonance study in humans. Neurosci Lett 271:29–32CrossRefPubMed
Zurück zum Zitat Huttunen J, Wikstrom H, Korvenoja A, Seppalainen AM, Aronen H, Ilmoniemi RJ (1996) Significance of the second somatosensory cortex in sensorimotor integration: enhancement of sensory responses during finger movements. Neuroreport 7(5):1009–12PubMed Huttunen J, Wikstrom H, Korvenoja A, Seppalainen AM, Aronen H, Ilmoniemi RJ (1996) Significance of the second somatosensory cortex in sensorimotor integration: enhancement of sensory responses during finger movements. Neuroreport 7(5):1009–12PubMed
Zurück zum Zitat Innocenti GM (1986) General organization of callosal connections in the cerebral cortex. In: Jones EG, Peters A (eds) Cerebral cortex. 5. Sensory-motor areas and aspects of cortical connectivity. Plenum, New York Innocenti GM (1986) General organization of callosal connections in the cerebral cortex. In: Jones EG, Peters A (eds) Cerebral cortex. 5. Sensory-motor areas and aspects of cortical connectivity. Plenum, New York
Zurück zum Zitat Iwamura Y (2000) Bilateral receptive field neurons and callosal connections in the somatosensory cortex. Phil Trans R Soc Lond B 355:267–273CrossRef Iwamura Y (2000) Bilateral receptive field neurons and callosal connections in the somatosensory cortex. Phil Trans R Soc Lond B 355:267–273CrossRef
Zurück zum Zitat James TW, Humphrey GK, Gati JS, Servos P, Menon RS, Goodale MA (2002) Haptic study of three-dimensional objects activates extrastriate visual areas. Neuropsychologica 40:1706–14CrossRef James TW, Humphrey GK, Gati JS, Servos P, Menon RS, Goodale MA (2002) Haptic study of three-dimensional objects activates extrastriate visual areas. Neuropsychologica 40:1706–14CrossRef
Zurück zum Zitat Jancke L, Loose R, Lutz K, Specht K, Shah NJ (2000) Cortical activations during paced finger tapping applying visual and auditory pacing stimuli. Cogn Brain Res 10:51–66CrossRef Jancke L, Loose R, Lutz K, Specht K, Shah NJ (2000) Cortical activations during paced finger tapping applying visual and auditory pacing stimuli. Cogn Brain Res 10:51–66CrossRef
Zurück zum Zitat Johansen-Berg H, Christensen V, Woolrich M, Matthews P (2000) Attention to touch modulates activity in both primary and secondary somatosensory areas. Neuroreport 11:1237–41PubMed Johansen-Berg H, Christensen V, Woolrich M, Matthews P (2000) Attention to touch modulates activity in both primary and secondary somatosensory areas. Neuroreport 11:1237–41PubMed
Zurück zum Zitat Karhu J, Tesche CD (1999) Simultaneous early processing of sensory input in human primary (SI) and secondary (SII) somatosensory cortices. J Neurophysiol 81(5):2017–25PubMed Karhu J, Tesche CD (1999) Simultaneous early processing of sensory input in human primary (SI) and secondary (SII) somatosensory cortices. J Neurophysiol 81(5):2017–25PubMed
Zurück zum Zitat Lutz K, Specht K, Shah NJ, Jancke L (2000) Tapping movements according to regular and irregular visual timing signals investigated with fMRI. Neuroreport 11(6):1301–6PubMed Lutz K, Specht K, Shah NJ, Jancke L (2000) Tapping movements according to regular and irregular visual timing signals investigated with fMRI. Neuroreport 11(6):1301–6PubMed
Zurück zum Zitat Manzoni T, Conti, F, Fabri M (1986) Callosal projections from area SII to SI in monkeys: anatomical organization and comparison with association projections. J Comp Neurol 252 (2):245–63 Manzoni T, Conti, F, Fabri M (1986) Callosal projections from area SII to SI in monkeys: anatomical organization and comparison with association projections. J Comp Neurol 252 (2):245–63
Zurück zum Zitat Matthews PBC (1988) Proprioceptors and their contribution to somatosensory mapping: complex messages require complex processing. Can J Physiol Pharmacol 66:430–438PubMed Matthews PBC (1988) Proprioceptors and their contribution to somatosensory mapping: complex messages require complex processing. Can J Physiol Pharmacol 66:430–438PubMed
Zurück zum Zitat Meyer E, Ferguson SS, Zatorre RJ, Alivisatos B, Marrett S, Evans AC, Hakim AM (1991) Attention modulates somatosensory cerebral blood flow response to vibrotactile stimulation as measured by positron emission tomography. Ann Neurol 29(4):440–3PubMed Meyer E, Ferguson SS, Zatorre RJ, Alivisatos B, Marrett S, Evans AC, Hakim AM (1991) Attention modulates somatosensory cerebral blood flow response to vibrotactile stimulation as measured by positron emission tomography. Ann Neurol 29(4):440–3PubMed
Zurück zum Zitat Mima T, Nagamine T, Nakamura K, Shibasaki H (1998) Attention modulates both primary and second somatosensory cortical activities in humans: a magnetoencephalographic study. J Neurophysiol 80(4):2215–21PubMed Mima T, Nagamine T, Nakamura K, Shibasaki H (1998) Attention modulates both primary and second somatosensory cortical activities in humans: a magnetoencephalographic study. J Neurophysiol 80(4):2215–21PubMed
Zurück zum Zitat Nelson RJ (1996) Interactions between motor commands and somatic perception in sensorimotor cortex. Curr Opin Neurobiol 6:801–810CrossRefPubMed Nelson RJ (1996) Interactions between motor commands and somatic perception in sensorimotor cortex. Curr Opin Neurobiol 6:801–810CrossRefPubMed
Zurück zum Zitat Rushworth MF, Nixon PD, Renowden S, Wade DT, Passingham RE (1997) The left parietal cortex and motor attention. Neuropsychologica 35:1261–73CrossRef Rushworth MF, Nixon PD, Renowden S, Wade DT, Passingham RE (1997) The left parietal cortex and motor attention. Neuropsychologica 35:1261–73CrossRef
Zurück zum Zitat Rushworth MF, Krams M, Passingham RE (2001) The attentional role of the left parietal cortex: the distinct lateralization and localization of motor attention in the human brain. J Cogn Neurosci 13:698–710CrossRefPubMed Rushworth MF, Krams M, Passingham RE (2001) The attentional role of the left parietal cortex: the distinct lateralization and localization of motor attention in the human brain. J Cogn Neurosci 13:698–710CrossRefPubMed
Zurück zum Zitat Sarter M, Givens B, Bruno JP (2001) The cognitive neuroscience of sustained attention: where top-down meets bottom-up. Brain Res Rev 35:146–160PubMed Sarter M, Givens B, Bruno JP (2001) The cognitive neuroscience of sustained attention: where top-down meets bottom-up. Brain Res Rev 35:146–160PubMed
Zurück zum Zitat Schnitzler A, Slamelin R, Salenius S, Jousmaki V, Hari T (1995) Tactile information from the human hand reaches the ipsilateral primary somatosensory cortex. Neurosci Let 200:25–28CrossRef Schnitzler A, Slamelin R, Salenius S, Jousmaki V, Hari T (1995) Tactile information from the human hand reaches the ipsilateral primary somatosensory cortex. Neurosci Let 200:25–28CrossRef
Zurück zum Zitat Shanks MF, Pearson RCA, Powell TPS (1985) The callosal connections of the primary somatic sensory cortex in the monkey. Brain Res Rev 9:43–65CrossRef Shanks MF, Pearson RCA, Powell TPS (1985) The callosal connections of the primary somatic sensory cortex in the monkey. Brain Res Rev 9:43–65CrossRef
Zurück zum Zitat Staines WR, Graham S, Black S, McIlroy WE (2002) Task-relevant modulation of primary somatosensory cortex is mediated via prefrontal cortical gating system. Neuroimage 15(1):190–199CrossRefPubMed Staines WR, Graham S, Black S, McIlroy WE (2002) Task-relevant modulation of primary somatosensory cortex is mediated via prefrontal cortical gating system. Neuroimage 15(1):190–199CrossRefPubMed
Zurück zum Zitat Steinmetz PN, Roy A, Fitzgerald PJ, Hsiao SS, Johnson KO, Neibur E (2000) Attention modulates synchronized neuronal firing pattern in primate somatosensory cortex. Nature 404(6774):187–190PubMed Steinmetz PN, Roy A, Fitzgerald PJ, Hsiao SS, Johnson KO, Neibur E (2000) Attention modulates synchronized neuronal firing pattern in primate somatosensory cortex. Nature 404(6774):187–190PubMed
Zurück zum Zitat Zangaladze A, Epstein CM, Grafton ST, Sathian K (1999) Involvement of visual cortex in tactile discrimination of orientation. Nature 401:587–590PubMed Zangaladze A, Epstein CM, Grafton ST, Sathian K (1999) Involvement of visual cortex in tactile discrimination of orientation. Nature 401:587–590PubMed
Metadaten
Titel
Tactile stimulus predictability modulates activity in a tactile-motor cortical network
verfasst von
A. J. Nelson
W. R. Staines
W. E. McIlroy
Publikationsdatum
01.01.2004
Erschienen in
Experimental Brain Research / Ausgabe 1/2004
Print ISSN: 0014-4819
Elektronische ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-003-1627-x

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