初级躯体感觉皮层是否参与疼痛的编码?
Whether the Primary Somatosensory Cortex Plays an Important Role in Pain Coding?
摘要: 疼痛是伴随实际或潜在的组织损伤,并令人产生不愉快的情绪和感觉体验,也是包括情绪-动机、感觉-辨别和认知-情感的多维度的复杂主观感受。由于初级躯体感觉皮层在疼痛编码中的作用一直存在争议,本文综述了关于初级躯体感觉皮层编码疼痛刺激部位、强度和性质的动物实验、非侵入性人类实验结合临床影像学研究等方面的研究论文,并就这些研究结果展开讨论,指出了导致目前结果差异可能的原因、局限性,并提出一些加以改善的建议。
Abstract: Pain is an unpleasant multidimensional experience associated with real or potential tissue dam-age, as well as a complex experience encompassing sensory-discriminative, affective-motivational and cognitive-emotional components. However, because it remains unclear for the role of the primary somatosensory cortex for encoding of the pain, this review mainly discusses the role of the primary somatosensory cortex for encoding the location, intensity and nature of pain stimulus from the animal studies, non-invasive brain damage studies combined with clinical imaging technologies. Finally, based on the current researches, we gave some possible reasons for the inconsistent results and the limitations of these studies, as well as put forward some suggestions that may be useful for the future study.
文章引用:李钻, 陈伟海 (2017). 初级躯体感觉皮层是否参与疼痛的编码?. 心理学进展, 7(4), 469-483. https://doi.org/10.12677/AP.2017.74058

参考文献

[1] Andersson, J. L., Lilja, A., Hartvig, P., Langstrom, B., Gordh, T., Handwerker, H., & Torebjork, E. (1997a). Somatotopic Organization along the Central Sulcus, for Pain Localization in Humans, as Revealed by Positron Emission Tomography. Experimental Brain Research, 117, 192-199.
[2] Apkarian, A. V., Bushnell, M. C., Treede, R. D., & Zubieta, J. K. (2005). Human Brain Mechanisms of Pain Perception and Regulation in Health and Disease. European Journal of Pain, 9, 463-484.
[3] Atlas, L. Y., & Wager, T. D. (2012). How Expectations Shape Pain. Neuroscience Letters, 520, 140-148.
[4] Bicket, M. C., Dunn, R. Y., & Ahmed, S. U. (2016). High-Frequency Spinal Cord Stimulation for Chronic Pain: Pre-Clinical Overview and Systematic Review of Controlled Trials. Pain Medicine, 17, 2326-2336.
https://doi.org/10.1093/pm/pnw156
[5] Bingel, U., Rose, M., Glascher, J., & Buchel, C. (2007). fMRI Reveals How Pain Modulates Visual Object Processing in the Ventral Visual Stream. Neuron, 55, 157-167.
[6] Bornhovd, K., Quante, M., Glauche, V., Bromm, B., Weiller, C., & Buchel, C. (2002). Painful Stimuli Evoke Different Stimulus-Response Functions in the Amygdala, Prefrontal, Insula and Somatosensory Cortex: A Single-Trial FMRI Study. Brain, 125, 1326-1336.
https://doi.org/10.1093/brain/awf137
[7] Bushnell, M. C., Duncan, G. H., Hofbauer, R. K., Ha, B., Chen, J. I., & Carrier, B. (1999). Pain Perception: Is There a Role for Primary Somatosensory Cortex? Proceedings of the National Academy of Sciences, 96, 7705-7709.
[8] Cai, Y. Q., Wang, W., Hou, Y. Y., & Pan, Z. Z. (2014). Optogenetic Activation of Brainstem Serotonergic Neurons Induces Persistent Pain Sensitization. Molecular Pain, 10, 70.
[9] Canavero, S. (2009). Textbook of Therapeutic Cortical Stimulation. New York, NY: Nova Biomedical Books.
[10] Canavero, S., & Bonicalzi, V. (2013). Role of Primary Somatosensory Cortex in the Coding of Pain. Pain, 154, 1156- 1158.
[11] Casey, K. L., Minoshima, S., Berger, K. L., Koeppe, R. A., Morrow, T. J., & Frey, K. A. (1994). Positron Emission Tomographic Analysis of Cerebral Structures Activated Specifically by Repetitive Noxious Heat Stimuli. Journal of Neurophysiology, 71, 802-807.
[12] Casey, K. L., Minoshima, S., Morrow, T. J., & Koeppe, R. A. (1996). Comparison of Human Cerebral Activation Pattern during Cutaneous Warmth, Heat Pain, and Deep Cold Pain. Journal of Neurophysiology, 76, 571-581.
[13] Cerkevich, C. M., Qi, H., & Kaas, J. H. (2014). Corticocortical Projections to Representations of the Teeth, Tongue, and Face in Somatosensory Area 3b of Macaques. Journal of Comparative Neurology, 522, 546-572.
https://doi.org/10.1002/cne.23426
[14] Chen, L. M., Friedman, R. M., & Roe, A. W. (2009). Area-Specific Representation of Mechanical Nociceptive Stimuli within SI Cortex of Squirrel Monkeys. Pain, 141, 258-268.
[15] Chudler, E. H., Anton, F., Dubner, R., & Kenshalo, D. J. (1990). Responses of Nociceptive SI Neurons in Monkeys and Pain Sensation in Humans Elicited by Noxious Thermal Stimulation: Effect of Interstimulus Interval. Journal of Neurophysiology, 63, 559-569.
[16] Della, P. S., Torquati, K., Pizzella, V., Babiloni, C., Franciotti, R., Rossini, P. M., & Romani, G. L. (2004). Temporal Dynamics of Alpha and Beta Rhythms in Human SI and SII after Galvanic Median Nerve Stimulation. A MEG Study. Neuroimage, 22, 1438-1446.
[17] Devonshire, I. M., Greenspon, C. M., & Hathway, G. J. (2015). Developmental Alterations in Noxious-Evoked EEG Activity Recorded from Rat Primary Somatosensory Cortex. Neuroscience, 305, 343-350.
[18] Disbrow, E., Buonocore, M., Antognini, J., Carstens, E., & Rowley, H. A. (1998). Somatosensory Cortex: A Comparison of the Response to Noxious Thermal, Mechanical, and Electrical Stimuli Using Functional Magnetic Resonance Imaging. Human Brain Mapping, 6, 150-159.
[19] Dykes, R., Metherate, R., & Tremblay, N. (1990). Transient and Prolonged Effects of Acetylcholine on Responsiveness of Cat Somatosensory Cortical Neurons. Journal of Neurophysiology, 63, 223.
[20] Eccleston, C., & Crombez, G. (1999). Pain Demands Attention: A Cognitive-Affective Model of the Interruptive Function of Pain. Psychological Bulletin, 125, 356-366.
[21] Eippert, F., Finsterbusch, J., Bingel, U., & Buchel, C. (2009). Direct Evidence for Spinal Cord Involvement in Placebo Analgesia. Science, 326, 404.
https://doi.org/10.1126/science.1180142
[22] Flor, H., Elbert, T., Knecht, S., Wienbruch, C., Pantev, C., Birbaumer, N., & Taub, E. (1995). Phantom-Limb Pain as a Perceptual Correlate of Cortical Reorganization Following Arm Amputation. Nature, 375, 482-484.
https://doi.org/10.1038/375482a0
[23] Follett, K. A., & Dirks, B. (1994). Characterization of Responses of Primary Somatosensory Cerebral Cortex Neurons to Noxious Visceral Stimulation in the Rat. Brain Research, 656, 27-32.
[24] Friston, K. (2003). Learning and Inference in the Brain. Neural Networks, 16, 1325-1352.
[25] Gazzola, V., Spezio, M. L., Etzel, J. A., Castelli, F., Adolphs, R., & Keysers, C. (2012). Primary Somatosensory Cortex Dis-criminates Affective Significance in Social Touch. Proceedings of the National Academy of Sciences, 109, E1657-E1666.
https://doi.org/10.1073/pnas.1113211109
[26] Gu, L., Uhelski, M. L., Anand, S., Romero-Ortega, M., Kim, Y., Fuchs, P. N., & Mohanty, S. K. (2015). Pain Inhibition by Optogenetic Activation of Specific Anterior Cingulate Cortical Neurons. PLoS ONE, 10, e117746.
https://doi.org/10.1371/journal.pone.0117746
[27] Guilbaud, G., Benoist, J. M., Levante, A., Gautron, M., & Willer, J. C. (1992). Primary Somatosensory Cortex in Rats with Pain-Related Behaviours Due to a Peripheral Mononeuropathy after Moderate Ligation of One Sciatic Nerve: Neuronal Responsivity to Somatic Stimulation. Experimental Brain Research, 92, 227-245.
https://doi.org/10.1007/bf00227967
[28] Hofbauer, R. K., Rainville, P., Duncan, G. H., & Bushnell, M. C. (2001). Cortical Representation of the Sensory Dimension of Pain. Journal of Neurophysiology, 86, 402-411.
[29] Hu, L., Cai, M. M., Xiao, P., Luo, F., & Iannetti, G. D. (2014). Human Brain Researchponses to Concomitant Stimulation of Adelta and C Nociceptors. Journal of Neuroscience, 34, 11439-11451.
[30] Hu, L., Xia, X. L., Peng, W. W., Su, W. X., Luo, F., Yuan, H., & Iannetti, G. (2015). Was It a Pain or a Sound? Across-Species Variability in Sensory Sensitivity. Pain, 156, 2449-2457.
https://doi.org/10.1097/j.pain.0000000000000316
[31] Hu, L., & Iannetti, G. D. (2016). Issues in Pain Predic-tion—Beyond Pain and Gain. Trends in Neurosciences, 39, 640- 642.
[32] Huang, G., Xiao, P., Hung, Y. S., Iannetti, G. D., Zhang, Z. G., & Hu, L. (2013). A Novel Approach to Predict Subjective Pain Perception from Single-Trial La-ser-Evoked Potentials. NeuroImage, 81, 283-293.
[33] Devonshire, C. M. G. A., & Hathway, G. J. (2004). Developmental Alterations in Noxious-Evoled EEG Activity Recorded from Rat Primary Somatosensory Cortex. Neuroscience, 305, 343-350.
[34] Jeong, J., McCall, J. G., Shin, G., Zhang, Y., Al-Hasani, R., Kim, M., & Rogers, J. A. (2015). Wireless Optofluidic Systems for Programmable in Vivo Pharmacology and Optogenetics. Cell, 162, 662-674.
[35] Johnson, C. (2016). Research Tools for the Measurement of Pain and Nociception. Animals, 6, 71.
https://doi.org/10.3390/ani6110071
[36] Jones, A. K., Brown, W. D., Friston, K. J., Qi, L. Y., & Frackowiak, R. S. (1991). Cortical and Subcortical Localization of Response to Pain in Man Using Positron Emission Tomography. Pro-ceedings. Biological sciences, 244, 39-44.
https://doi.org/10.1098/rspb.1991.0048
[37] Kenshalo, D. J., Chudler, E. H., Anton, F., & Dubner, R. (1988a). SI Nociceptive Neurons Participate in the Encoding Process by Which Monkeys Perceive the Intensity of Noxious Thermal Stimulation. Brain Research, 454, 378-382.
[38] Kenshalo, D. J., & Isensee, O. (1983a). Responses of Primate SI Cortical Neurons to Noxious Stimuli. Journal of Neurophysiology, 50, 1479-1496.
[39] Khatibi, A., Vachon-Presseau, E., Schrooten, M., Vlaeyen, J., & Rainville, P. (2014). Attention Effects on Vicarious Modulation of Nociception and Pain. Pain, 155, 2033-2039.
[40] Kiritoshi, T., Ji, G., & Neugebauer, V. (2016). Rescue of Impaired mGluR5-Driven Endocannabinoid Signaling Restores Prefrontal Cortical Output to Inhibit Pain in Arthritic Rats. Journal of Neuroscience, 36, 837-850.
https://doi.org/10.1523/JNEUROSCI.4047-15.2016
[41] Knecht, M., & Lidzba, K. (2016). Processing Verbal Morphology in Patients with Congenital Left-Hemispheric Brain Lesions. Brain Lang, 157-158, 25-34.
[42] Lee, G. H., & Kim, S. S. (2016). Therapeutic Strategies for Neuropathic Pain: Potential Application of Pharmacosynthetics and Optogenetics. Mediators of Inflammation, 2016, Article ID: 5808215.
[43] Lee, M., Manders, T. R., Eberle, S. E., Su, C., D’Amour, J., Yang, R., & Wang, J. (2015). Activation of Corticostriatal Circuitry Relieves Chronic Neuropathic Pain. Journal of Neuroscience, 35, 5247-5259.
https://doi.org/10.1523/JNEUROSCI.3494-14.2015
[44] Loeser, J. D., & Treede, R. D. (2008). The Kyoto protocol of IASP Basic Pain Terminology. Pain, 137, 473-477.
[45] Luo, Z., Yu, M., Smith, S. D., Kritzer, M., Du, C., Ma, Y., & Benveniste, H. (2009). The Effect of Intravenous Lidocaine on Brain Activation during Non-Noxious and Acute Noxious Stimulation of the Forepaw: A Functional Magnetic Resonance Imaging Study in the Rat. Anesthesia & Analgesia, 108, 334-344.
https://doi.org/10.1213/ane.0b013e31818e0d34
[46] Mathieu, L. (2016). Assessing a Patient’s Pain. Soins, 61, 14-17.
[47] Moulton, E. A., Keaser, M. L., Gullapalli, R. P., & Greenspan, J. D. (2005). Regional Intensive and Temporal Patterns of Functional MRI Activation Distinguishing Noxious and Innocuous Contact Heat. Journal of Neurophysiology, 93, 2183-2193.
[48] Murrell, J. C., Mitchinson, S. L., Waters, D., & Johnson, C. B. (2007). Comparative Effect of Thermal, Mechanical, and Electrical Noxious Stimuli on the Electroencephalogram of the Rat. British Journal of Anaesthesia, 98, 366-371.
https://doi.org/10.1093/bja/ael377
[49] Nakata, H., Tamura, Y., Sakamoto, K., Akatsuka, K., Hirai, M., Inui, K., & Kakigi, R. (2008). Evoked Magnetic Fields Following Noxious Laser Stimulation of the Thigh in Humans. Neuroimage, 42, 858-868.
[50] Peirs, C., & Seal, R. P. (2016). Neural Circuits for Pain: Recent Advances and Current Views. Science, 354, 578-584.
[51] Peyron, R., Laurent, B., & Garcia-Larrea, L. (2000). Functional Imaging of Brain Research Ponses to Pain. A Review and Meta-Analysis. Neurophysiologie Clinique, 30, 263-288.
[52] Pleger, B., Draganski, B., Schwenkreis, P., Lenz, M., Nicolas, V., Maier, C., & Tegenthoff, M. (2014). Complex Regional Pain Syndrome Type I Affects Brain Structure in Prefrontal and Motor Cortex. PLoS ONE, 9, e85372.
[53] Ploner, M., Freund, H. J., & Schnitzler, A. (1999). Pain Affect without Pain Sensation in a Patient with a Postcentral Lesion. Pain, 81, 211-214.
[54] Ploner, M., Schmitz, F., Freund, H. J., & Schnitzler, A. (1999). Parallel Activation of Primary and Secondary Somatosensory Cortices in Human Pain Processing. Journal of Neurophysiology, 81, 3100-3104.
[55] Quiton, R. L., Masri, R., Thompson, S. M., & Keller, A. (2010). Abnormal Activity of Primary Somatosensory Cortex in Central Pain Syndrome. Journal of Neurophysiology, 104, 1717-1725.
https://doi.org/10.1152/jn.00161.2010
[56] Raij, T. T., Forss, N., Stanck, A., & Hari, R. (2004). Modulation of Motor-Cortex Oscillatory Activity by Painful A- and C-Fiber Stimuli. NeuroImage, 23, 569-573.
[57] Rainville, P., Bao, Q. V., & Chretien, P. (2005). Pain-Related Emotions Modulate Experimental Pain Perception and Autonomic Responses. Pain, 118, 306-318.
[58] Rao, J. S., Manxiu, M., Zhao, C., Xi, Y., Yang, Z. Y., Zuxiang, L., & Li, X. G. (2013). Atrophy and Primary Somatosensory Cortical Reorganization after Unilateral Thoracic Spinal Cord Injury: A Longitudinal Functional Magnetic Resonance Imaging Study. BioMed Research International, 2013, Article ID: 753061.
[59] Reed, J. L., Pouget, P., Qi, H. X., Zhou, Z., Bernard, M. R., Burish, M. J., & Kaas, J. H. (2012). Effects of Spatiotemporal Stimulus Properties on Spike Timing Correlations in Owl Monkey Primary Somatosensory Cortex. Journal of Neurophysiology, 108, 3353-3369.
[60] Schnitzler, A. (2000). Neurophysiology and Functional Neuroimaging of the Somatosensory System. Journal of Clinical Neurophysiology, 17, 537-538.
https://doi.org/10.1097/00004691-200011000-00001
[61] Schnitzler, A., Genet, F., Durand, M. C., Roche, N., Bensmail, D., Chartier-Kastler, E., & Denys, P. (2011). Pilot Study Evaluating the Safety of Intradetrusor Injections of Botulinum Toxin Type A: Investigation of Generalized Spread Using Single-Fiber EMG. Neurourology and Urodynamics, 30, 1533-1537.
https://doi.org/10.1002/nau.21103
[62] Talbot, J. D., Marrett, S., Evans, A. C., Meyer, E., Bushnell, M. C., & Duncan, G. H. (1991). Multiple Representations of Pain in Human Cerebral Cortex. Science, 251, 1355-1358.
https://doi.org/10.1126/science.2003220
[63] Tamaddonfard, E., & Hamzeh-Gooshchi, N. (2014). Effects of Administration of Histamine and Its H1, H2, and H3 Receptor Antagonists into the Primary Somatosensory Cortex on Inflammatory Pain in Rats. Iranian Journal of Basic Medical Sciences, 17, 55-61.
[64] Timmermann, L., Ploner, M., Haucke, K., Schmitz, F., Baltissen, R., & Schnitzler, A. (2001). Differential Coding of Pain Intensity in the Human Primary and Secondary Somatosensory Cortex. Journal of Neurophysiology, 86, 1499- 1503.
[65] Tommerdahl, M., Favorov, O. V., & Whitsel, B. L. (2005). Effects of High-Frequency Skin Stimulation on SI Cortex: Mechanisms and Functional Implications. Somatosensory & Motor Research, 22, 151-169.
https://doi.org/10.1080/08990220500084461
[66] Tommerdahl, M., Favorov, O. V., & Whitsel, B. L. (2010). Dynamic Representations of the Somatosensory Cortex. Neuroscience & Biobehavioral Reviews, 34, 160-170.
[67] Tracey, I., & Mantyh, P. W. (2007a). The Cerebral Signature for Pain Perception and Its Modulation. Neuron, 55, 377- 391.
[68] Treede, R. D., Kenshalo, D. R., Gracely, R. H., & Jones, A. K. (1999). The Cortical Representation of Pain. Pain, 79, 105-111.
[69] Vaz, S., Ferreira, T. C., Salgado, L., & Paycha, F. (2016). Bone Scan Usefulness in Patients with Painful Hip or Knee Prosthesis: 10 Situations That Can Cause Pain, Other than Loosening and Infection. European Journal of Orthopaedic Surgery & Traumatology, 27, 147-156.
[70] Vierck, C. J., Whitsel, B. L., Favorov, O. V., Brown, A. W., & Tommerdahl, M. (2013). Role of Primary Somatosensory Cortex in the Coding of Pain. Pain, 154, 334-344.
[71] Xia, X. L., Peng, W. W., Iannetti, G. D., & Hu, L. (2016). Laser-Evoked Cortical Responses in Freely-Moving Rats Reflect the Activation of C-Fibre Afferent Pathways. Neuroimage, 128, 209-217.
[72] Xie, G., Piche, M., Khoshnejad, M., Perlbarg, V., Chen, J. I., Hoge, R. D., & Cohen-Adad, J. (2012). Reduction of Physiological Noise with Independent Component Analysis Improves the Detection of Nociceptive Responses with fMRI of the Human Spinal Cord. Neuroimage, 63, 245-252.
[73] Xie, Y. F., Huo, F. Q., & Tang, J. S. (2009). Cerebral Cortex Modulation of Pain. Acta Pharmacologica Sinica, 30, 31- 41.
https://doi.org/10.1038/aps.2008.14
[74] Zemel, L., & Blier, P. R. (2016). Juvenile Fibromyalgia: A Primary Pain, or Pain Processing, Disorder. Seminars in Pediatric Neurology, 23, 231-241.
[75] Zhang, Y., Wang, N., Wang, J. Y., Chang, J. Y., Woodward, D. J., & Luo, F. (2011). Ensemble Encoding of Nociceptive Stimulus Intensity in the Rat Medial and Lateral Pain Systems. Molecular Pain, 7, 64.
https://doi.org/10.1186/1744-8069-7-64