Cerebral columnar organization of the first nociceptive component induced by CO2 laser on the tail of the rat

Fu-Shan Jaw; Yu-Chieh Jill Kao; Chih-Ping Chen; Wen-Li Liao

doi:10.1016/j.neuroscience.2008.09.046

Cerebral columnar organization of the first nociceptive component induced by CO2 laser on the tail of the rat

Fu-Shan Jaw, Yu-Chieh Jill Kao, Chih-Ping Chen, Wen-Li Liao

研究成果: 雜誌貢獻 › 文章 › 同行評審

5 引文斯高帕斯（Scopus）

摘要

The somatotopic map of the first nociceptive component in the primary somatosensory cortex (S1) is still unclear. In this study, a CO2 laser was applied to the tail of the rat to induce nociception without the interference from large myelinated (Aβ) fibers. Thus, only noxious fibers could be activated. Two-dimensional current-source-density analysis was used to analyze the evoked field potentials. Using this method, the nociceptive responses of Aδ-fibers in S1 were verified, and the somatotopic map of the first nociceptive component in S1 was identified. We found that whether light touch or laser-induced nociception was applied to the tail of the rat, the responsive topography in S1 was consistent. Discrimination of these two modalities was achieved vertically in the same column; the deeper layer represented the nociceptive response while the superficial layer encoded the response to light touch. This is quite different from that of a primate brain. © 2009 IBRO.

原文	英語
頁（從 - 到）	945-950
頁數	6
期刊	Neuroscience
卷	158
發行號	2
DOIs	https://doi.org/10.1016/j.neuroscience.2008.09.046
出版狀態	已發佈 - 2009
對外發佈	是

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10.1016/j.neuroscience.2008.09.046

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@article{12c9ef256cea45a5a6045ae99d673521,

title = "Cerebral columnar organization of the first nociceptive component induced by CO2 laser on the tail of the rat",

abstract = "The somatotopic map of the first nociceptive component in the primary somatosensory cortex (S1) is still unclear. In this study, a CO2 laser was applied to the tail of the rat to induce nociception without the interference from large myelinated (Aβ) fibers. Thus, only noxious fibers could be activated. Two-dimensional current-source-density analysis was used to analyze the evoked field potentials. Using this method, the nociceptive responses of Aδ-fibers in S1 were verified, and the somatotopic map of the first nociceptive component in S1 was identified. We found that whether light touch or laser-induced nociception was applied to the tail of the rat, the responsive topography in S1 was consistent. Discrimination of these two modalities was achieved vertically in the same column; the deeper layer represented the nociceptive response while the superficial layer encoded the response to light touch. This is quite different from that of a primate brain. {\textcopyright} 2009 IBRO.",

keywords = "CO2 laser, cortex, current source density, evoked potentials, nociception, rat tail, carbon dioxide, afferent nerve group 1, animal experiment, article, brain mapping, controlled study, electric potential, evoked response, laser, male, nerve fiber Adelta, nonhuman, priority journal, rat, somatosensory cortex, tactile stimulation, Animals, Brain Mapping, Electroencephalography, Evoked Potentials, Somatosensory, Lasers, Gas, Male, Nerve Fibers, Myelinated, Neural Conduction, Pain, Pain Measurement, Physical Stimulation, Rats, Rats, Wistar, Reaction Time, Somatosensory Cortex, Tail",

author = "Fu-Shan Jaw and Kao, {Yu-Chieh Jill} and Chih-Ping Chen and Wen-Li Liao",

note = "被引用次數：4 Export Date: 6 April 2016 CODEN: NRSCD 通訊地址: Jaw, F.-S.; Institute of Biomedical Engineering, National Taiwan University, No.1, Sec. 4, Roosevelt Rd, Taipei, 10617, Taiwan; 電子郵件： jaw@ntu.edu.tw 化學物質/CAS: carbon dioxide, 124-38-9, 58561-67-4 參考文獻: Apkarian, A.V., Stevens, R.T., Jones, M.W., Hodge, J., Cells of origin of the spinothalamic pathways in the primate (1987) Pain, 30, pp. S398; Bodor, A.L., Katona, I., Nyiri, G., Mackie, K., Ledent, C., Hajos, N., Freund, T.F., Endocannabinoid signaling in rat somatosensory cortex: laminar differences and involvement of specific interneuron types (2005) J Neurosci, 25, pp. 6845-6856; Bornhovd, K., Quate, M., Galuche, V., Bromm, B., Weiller, C., Buchel, C., Painful stimuli evoke different stimulus-response functions in the amygdale, prefrontal, insula and somatosensory cortex: a single-trial fMRI study (2002) Brain, 125, pp. 1326-1336; Bromm, B., Treede, R.D., Nerve fiber discharges, cerebral potentials and sensations induced by CO2 laser stimulation (1984) Hum Neurobiol, 3, pp. 33-40; Bromm, B., Chen, C.A.N., Brain electrical source analysis of laser evoked potentials in response to painful trigeminal nerve stimulation (1995) Electroencephalogr Clin Neurophysiol, 95, pp. 12-26; Bromm, B., Lorenz, J., Neurophysiological evaluation of pain (1998) Electroencephalogr Clin Neurophysiol, 107, pp. 227-253; Cauli, B., Audinat, E., Lambolez, B., Angulo, M.C., Ropert, N., Tsuzuki, K., Hestrin, S., Rossier, J., Molecular and physiological diversity of cortical non-pyramidal cells (1997) J Neurosci, 17, pp. 3894-3906; Chien, C.N., Li, J.Y., Jaw, F.S., Pseudo-synchronous system for recording action and field potentials simultaneously (2007) Measurement, 40, pp. 717-723; Craig, A.D., Pain mechanism: labeled lines versus convergence in central processing (2003) Annu Rev Neurosci, 26, pp. 1-30; Hofbauer, R.K., Rainville, P., Duncan, G.H., Bushnell, M.C., Cortical representation of the sensory dimension of pain (2001) J Neurophysiol, 86, pp. 402-411; Horton, J.C., Adams, D.L., The cortical column: a structure without a function (2005) Philos Trans R Soc B, 360, pp. 837-862; Horton, J.C., Hocking, D.R., Monocular core zones and binocular border strips in primate striate cortex revealed by the contrasting effects of enucleation, eyelid suture, and retinal laser lesions on cytochrome oxidase activity (1998) J Neurosci, 18, pp. 5433-5455; Jaw, F.S., Optimal sampling of electrophysiological signals (2001) Neurosci Res Commun, 28, pp. 75-84; Jaw, F.S., Kao, Y.C., Chen, C.P., Lee, C.Y., Chen, Y.Y., High-fidelity evoked potential for mapping the rat tail in thalamus (2008) Neuroscience, 155 (1), pp. 277-282; Kalliomaki, J., Weng, H.R., Nilsson, H.J., Schouenburg, J., Nociceptive C fiber input to the primary somatosensory cortex (S1). A field potential study in the rat (1993) Brain Res, 622, pp. 262-270; Lamour, Y., Willer, J.C., Guilbaut, G., Rat somatosensory (Sm1) cortex: I. Characteristics of neuronal responses to noxious stimulation and comparison with non-noxious stimulation (1983) Exp Brain Res, 49, pp. 35-45; Lamour, Y., Guilbaut, G., Willer, J.C., Rat somatosensory (Sm1) cortex: II. Laminar and columnar organization of noxious and non-noxious inputs (1983) Exp Brain Res, 49, pp. 46-54; LeVay, S., Nelson, S.B., Columnar organization of the visual cortex (1991) The neural basis of visual function, pp. 266-315. , Leventhal A.G. (Ed), CRC Press, Boston; Lorento De No, R., Cerebral cortex: architecture, intracortical connections, motor projections (1949) Physiology of the nervous system, pp. 288-330. , Fulton J. (Ed), Oxford University Press, New York; Mountcastle, V.B., Berman, A.L., Davies, P.W., Topographic organization and modality representation in first somatic area of cat's cerebral cortex to peripheral stimuli (1955) Am J Physiol, 183, p. 464; Mountcastle, V.B., The columnar organization of the neocortex (1997) Brain, 120, pp. 701-722; Nicholls, J.H., Martin, A.R., Wallace, B.G., Fuchs, P.A., (2001) From neuron to brain. 4th edition, , Massachusetts Press, Sunderland; Ohara, S., Crone, N.E., Weiss, N., Treede, R.D., Lenz, F.A., Amplitudes of laser evoked potential recorded from primary somatosensory, parasylvian and medial frontal cortex are graded with stimulus intensity (2004) Pain, 110, pp. 318-328; Rakic, P., Guidance of neurons migration to the fetal monkey neocortex (1971) Brain Res, 33, pp. 471-476; Rakic, P., Specification of cerebral cortical areas (1988) Science, 241, pp. 170-176; Salin, P.A., Prince, D.A., Spontaneous GABAA receptor-mediated inhibitory currents in adult rat somatosensory cortex (1996) J Neurophysiol, 75, pp. 1573-1588; Schouenborg, J., Kalliomaki, J., Gustavsson, P., Rosen, I., Field potentials evoked in rat primary somatosensory cortex (S1) by impulses in cutaneous Aβ- and C-fibers (1986) Brain Res, 397, pp. 86-92; Shaw, F.Z., Chen, R.F., Tsao, H.W., Yen, C.T., Comparison of touch- and laser heat-evoked cortical field potentials in conscious rats (1999) Brain Res, 824, pp. 183-196; Shaw, F.Z., Chen, R.F., Yen, C.T., Dynamic changes of touch- and laser-evoked field potentials of primary somatosensory cortex in awake and pentobarbital-anesthetized rats (2001) Brain Res, 911, pp. 105-115; Sincich, L.C., Horton, J.C., An albino-like decussation error in the optic chiasm revealed by anomalous ocular dominance columns (2003) J Neurosci, 23, pp. 5684-5692; Sun, J.J., Yang, J.W., Shyu, B.C., Current source density analysis of laser heat-evoked intra-cortical field potentials in the primary somatosensory cortex of rats (2006) Neuroscience, 140, pp. 1321-1336; Tarkka, I.M., Treede, R.D., Equivalent electrical source analysis of pain-related somatosensory evoked potentials elicited by a CO2 laser (1993) J Clin Neurophysiol, 10, pp. 513-519; Tommerdahl, M., Delemos, K.A., Vierck, C.J., Favorov, O.V., Whitsel, B.L., Anterior parietal cortical response to tactile and skin-heating stimuli applied to the same skin site (1996) J Neurophysiol, 75, pp. 2662-2670; Treede, R.D., Kenshalo, D.R., Gracely, R.H., Jones, A.K.P., The cortical representation of pain (1999) Pain, 79, pp. 105-111; Valeriani, M., Barba, C., Le Pera, D., Restuccia, D., Colicchio, G., Tonali, P., Gagliardo, O., Treed, R.F., Different neuronal contribution to N20 somatosensory evoked potential and to CO2 laser evoked potentials: an intracerebral recording study (2004) Clin Neurophysiol, 115, pp. 211-216; Walsh, C., Cepko, C.L., Widespread dispersion of neuronal clones across functional regions of the cerebral cortex (1992) Science, 255, pp. 434-440; White, E.L., Keller, A., An integrative view of cortical circuitry (1989) Cortical circuits: synaptic organization of the cerebral cortex; structure, function, and theory, pp. 179-206. , White E.L. (Ed), Birkhauser Publisher, Boston; Zhang, Z.W., Deschenes, M., Intracortical axonal projections of lamina VI cells of the primary somatosensory cortex in the rat: a single-cell labeling study (1997) J Neurosci, 17, pp. 6365-6379",

year = "2009",

doi = "10.1016/j.neuroscience.2008.09.046",

language = "English",

volume = "158",

pages = "945--950",

journal = "Neuroscience",

issn = "0306-4522",

publisher = "Elsevier Ireland Ltd",

number = "2",

}

TY - JOUR

T1 - Cerebral columnar organization of the first nociceptive component induced by CO2 laser on the tail of the rat

AU - Jaw, Fu-Shan

AU - Kao, Yu-Chieh Jill

AU - Chen, Chih-Ping

AU - Liao, Wen-Li

N1 - 被引用次數：4 Export Date: 6 April 2016 CODEN: NRSCD 通訊地址: Jaw, F.-S.; Institute of Biomedical Engineering, National Taiwan University, No.1, Sec. 4, Roosevelt Rd, Taipei, 10617, Taiwan; 電子郵件： jaw@ntu.edu.tw 化學物質/CAS: carbon dioxide, 124-38-9, 58561-67-4 參考文獻: Apkarian, A.V., Stevens, R.T., Jones, M.W., Hodge, J., Cells of origin of the spinothalamic pathways in the primate (1987) Pain, 30, pp. S398; Bodor, A.L., Katona, I., Nyiri, G., Mackie, K., Ledent, C., Hajos, N., Freund, T.F., Endocannabinoid signaling in rat somatosensory cortex: laminar differences and involvement of specific interneuron types (2005) J Neurosci, 25, pp. 6845-6856; Bornhovd, K., Quate, M., Galuche, V., Bromm, B., Weiller, C., Buchel, C., Painful stimuli evoke different stimulus-response functions in the amygdale, prefrontal, insula and somatosensory cortex: a single-trial fMRI study (2002) Brain, 125, pp. 1326-1336; Bromm, B., Treede, R.D., Nerve fiber discharges, cerebral potentials and sensations induced by CO2 laser stimulation (1984) Hum Neurobiol, 3, pp. 33-40; Bromm, B., Chen, C.A.N., Brain electrical source analysis of laser evoked potentials in response to painful trigeminal nerve stimulation (1995) Electroencephalogr Clin Neurophysiol, 95, pp. 12-26; Bromm, B., Lorenz, J., Neurophysiological evaluation of pain (1998) Electroencephalogr Clin Neurophysiol, 107, pp. 227-253; Cauli, B., Audinat, E., Lambolez, B., Angulo, M.C., Ropert, N., Tsuzuki, K., Hestrin, S., Rossier, J., Molecular and physiological diversity of cortical non-pyramidal cells (1997) J Neurosci, 17, pp. 3894-3906; Chien, C.N., Li, J.Y., Jaw, F.S., Pseudo-synchronous system for recording action and field potentials simultaneously (2007) Measurement, 40, pp. 717-723; Craig, A.D., Pain mechanism: labeled lines versus convergence in central processing (2003) Annu Rev Neurosci, 26, pp. 1-30; Hofbauer, R.K., Rainville, P., Duncan, G.H., Bushnell, M.C., Cortical representation of the sensory dimension of pain (2001) J Neurophysiol, 86, pp. 402-411; Horton, J.C., Adams, D.L., The cortical column: a structure without a function (2005) Philos Trans R Soc B, 360, pp. 837-862; Horton, J.C., Hocking, D.R., Monocular core zones and binocular border strips in primate striate cortex revealed by the contrasting effects of enucleation, eyelid suture, and retinal laser lesions on cytochrome oxidase activity (1998) J Neurosci, 18, pp. 5433-5455; Jaw, F.S., Optimal sampling of electrophysiological signals (2001) Neurosci Res Commun, 28, pp. 75-84; Jaw, F.S., Kao, Y.C., Chen, C.P., Lee, C.Y., Chen, Y.Y., High-fidelity evoked potential for mapping the rat tail in thalamus (2008) Neuroscience, 155 (1), pp. 277-282; Kalliomaki, J., Weng, H.R., Nilsson, H.J., Schouenburg, J., Nociceptive C fiber input to the primary somatosensory cortex (S1). A field potential study in the rat (1993) Brain Res, 622, pp. 262-270; Lamour, Y., Willer, J.C., Guilbaut, G., Rat somatosensory (Sm1) cortex: I. Characteristics of neuronal responses to noxious stimulation and comparison with non-noxious stimulation (1983) Exp Brain Res, 49, pp. 35-45; Lamour, Y., Guilbaut, G., Willer, J.C., Rat somatosensory (Sm1) cortex: II. Laminar and columnar organization of noxious and non-noxious inputs (1983) Exp Brain Res, 49, pp. 46-54; LeVay, S., Nelson, S.B., Columnar organization of the visual cortex (1991) The neural basis of visual function, pp. 266-315. , Leventhal A.G. (Ed), CRC Press, Boston; Lorento De No, R., Cerebral cortex: architecture, intracortical connections, motor projections (1949) Physiology of the nervous system, pp. 288-330. , Fulton J. (Ed), Oxford University Press, New York; Mountcastle, V.B., Berman, A.L., Davies, P.W., Topographic organization and modality representation in first somatic area of cat's cerebral cortex to peripheral stimuli (1955) Am J Physiol, 183, p. 464; Mountcastle, V.B., The columnar organization of the neocortex (1997) Brain, 120, pp. 701-722; Nicholls, J.H., Martin, A.R., Wallace, B.G., Fuchs, P.A., (2001) From neuron to brain. 4th edition, , Massachusetts Press, Sunderland; Ohara, S., Crone, N.E., Weiss, N., Treede, R.D., Lenz, F.A., Amplitudes of laser evoked potential recorded from primary somatosensory, parasylvian and medial frontal cortex are graded with stimulus intensity (2004) Pain, 110, pp. 318-328; Rakic, P., Guidance of neurons migration to the fetal monkey neocortex (1971) Brain Res, 33, pp. 471-476; Rakic, P., Specification of cerebral cortical areas (1988) Science, 241, pp. 170-176; Salin, P.A., Prince, D.A., Spontaneous GABAA receptor-mediated inhibitory currents in adult rat somatosensory cortex (1996) J Neurophysiol, 75, pp. 1573-1588; Schouenborg, J., Kalliomaki, J., Gustavsson, P., Rosen, I., Field potentials evoked in rat primary somatosensory cortex (S1) by impulses in cutaneous Aβ- and C-fibers (1986) Brain Res, 397, pp. 86-92; Shaw, F.Z., Chen, R.F., Tsao, H.W., Yen, C.T., Comparison of touch- and laser heat-evoked cortical field potentials in conscious rats (1999) Brain Res, 824, pp. 183-196; Shaw, F.Z., Chen, R.F., Yen, C.T., Dynamic changes of touch- and laser-evoked field potentials of primary somatosensory cortex in awake and pentobarbital-anesthetized rats (2001) Brain Res, 911, pp. 105-115; Sincich, L.C., Horton, J.C., An albino-like decussation error in the optic chiasm revealed by anomalous ocular dominance columns (2003) J Neurosci, 23, pp. 5684-5692; Sun, J.J., Yang, J.W., Shyu, B.C., Current source density analysis of laser heat-evoked intra-cortical field potentials in the primary somatosensory cortex of rats (2006) Neuroscience, 140, pp. 1321-1336; Tarkka, I.M., Treede, R.D., Equivalent electrical source analysis of pain-related somatosensory evoked potentials elicited by a CO2 laser (1993) J Clin Neurophysiol, 10, pp. 513-519; Tommerdahl, M., Delemos, K.A., Vierck, C.J., Favorov, O.V., Whitsel, B.L., Anterior parietal cortical response to tactile and skin-heating stimuli applied to the same skin site (1996) J Neurophysiol, 75, pp. 2662-2670; Treede, R.D., Kenshalo, D.R., Gracely, R.H., Jones, A.K.P., The cortical representation of pain (1999) Pain, 79, pp. 105-111; Valeriani, M., Barba, C., Le Pera, D., Restuccia, D., Colicchio, G., Tonali, P., Gagliardo, O., Treed, R.F., Different neuronal contribution to N20 somatosensory evoked potential and to CO2 laser evoked potentials: an intracerebral recording study (2004) Clin Neurophysiol, 115, pp. 211-216; Walsh, C., Cepko, C.L., Widespread dispersion of neuronal clones across functional regions of the cerebral cortex (1992) Science, 255, pp. 434-440; White, E.L., Keller, A., An integrative view of cortical circuitry (1989) Cortical circuits: synaptic organization of the cerebral cortex; structure, function, and theory, pp. 179-206. , White E.L. (Ed), Birkhauser Publisher, Boston; Zhang, Z.W., Deschenes, M., Intracortical axonal projections of lamina VI cells of the primary somatosensory cortex in the rat: a single-cell labeling study (1997) J Neurosci, 17, pp. 6365-6379

PY - 2009

Y1 - 2009

N2 - The somatotopic map of the first nociceptive component in the primary somatosensory cortex (S1) is still unclear. In this study, a CO2 laser was applied to the tail of the rat to induce nociception without the interference from large myelinated (Aβ) fibers. Thus, only noxious fibers could be activated. Two-dimensional current-source-density analysis was used to analyze the evoked field potentials. Using this method, the nociceptive responses of Aδ-fibers in S1 were verified, and the somatotopic map of the first nociceptive component in S1 was identified. We found that whether light touch or laser-induced nociception was applied to the tail of the rat, the responsive topography in S1 was consistent. Discrimination of these two modalities was achieved vertically in the same column; the deeper layer represented the nociceptive response while the superficial layer encoded the response to light touch. This is quite different from that of a primate brain. © 2009 IBRO.

AB - The somatotopic map of the first nociceptive component in the primary somatosensory cortex (S1) is still unclear. In this study, a CO2 laser was applied to the tail of the rat to induce nociception without the interference from large myelinated (Aβ) fibers. Thus, only noxious fibers could be activated. Two-dimensional current-source-density analysis was used to analyze the evoked field potentials. Using this method, the nociceptive responses of Aδ-fibers in S1 were verified, and the somatotopic map of the first nociceptive component in S1 was identified. We found that whether light touch or laser-induced nociception was applied to the tail of the rat, the responsive topography in S1 was consistent. Discrimination of these two modalities was achieved vertically in the same column; the deeper layer represented the nociceptive response while the superficial layer encoded the response to light touch. This is quite different from that of a primate brain. © 2009 IBRO.

KW - CO2 laser

KW - cortex

KW - current source density

KW - evoked potentials

KW - nociception

KW - rat tail

KW - carbon dioxide

KW - afferent nerve group 1

KW - animal experiment

KW - article

KW - brain mapping

KW - controlled study

KW - electric potential

KW - evoked response

KW - laser

KW - male

KW - nerve fiber Adelta

KW - nonhuman

KW - priority journal

KW - rat

KW - somatosensory cortex

KW - tactile stimulation

KW - Animals

KW - Brain Mapping

KW - Electroencephalography

KW - Evoked Potentials, Somatosensory

KW - Lasers, Gas

KW - Male

KW - Nerve Fibers, Myelinated

KW - Neural Conduction

KW - Pain

KW - Pain Measurement

KW - Physical Stimulation

KW - Rats

KW - Rats, Wistar

KW - Reaction Time

KW - Somatosensory Cortex

KW - Tail

U2 - 10.1016/j.neuroscience.2008.09.046

DO - 10.1016/j.neuroscience.2008.09.046

M3 - Article

SN - 0306-4522

VL - 158

SP - 945

EP - 950

JO - Neuroscience

JF - Neuroscience

IS - 2

ER -

Cerebral columnar organization of the first nociceptive component induced by CO2 laser on the tail of the rat

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