串行处理还是并行处理?触觉信息在丘脑–体感皮层网络上的加工方式
Serial or Parallel Processing? The Processing of Tactile Information in the Network between Thalamus andSomatosensory Cortices

作者: 武广起 , 夏晓磊 :西南大学心理学部,认知与人格教育部重点实验室,重庆; 胡 理 :西南大学心理学部,认知与人格教育部重点实验室,重庆;中国科学院心理研究所,北京 ;

关键词: 触觉丘脑–体感皮层网络串行加工并行加工Tactile The Network between Thalamus and Somatosensory Cortices Serial Processing Parallel Processing

摘要:
触觉信息在丘脑–体感皮层网络上的加工方式目前主要存在两种相对立的理论:串行加工理论与并行加工理论。串行加工理论认为触觉信息是从丘脑传输到初级躯体感觉皮层(primary somatosensory cortex, S1),然后再从S1传输到次级躯体感觉皮层(secondary somatosensory cortex, S2);并行加工理论认为触觉信息是从丘脑同时并行传输到S1与S2。在加工触觉信息时,非灵长类与低等灵长类动物丘脑–体感皮层网络的加工方式通常被认为是并行的,而高等灵长类动物与人类丘脑–体感皮层网络的加工方式目前还存有争议。现有研究结果的争议主要源于刺激方式、采集技术和数据分析方法等多方面的局限性。在现有技术条件下,应强化实验设计,从自上而下的调节因素、脑可塑性等方面进一步研究触觉信息在丘脑–体感皮层网络上的加工方式。

Abstract: There are two conflicting theories regarding the processing of tactile information in the network between thalamus and somatosensory cortices: the serial and the parallel processing theories. The serial processing theory assumes that tactile information is transmitted from the thalamus to the primary somatosensory cortex (S1) and from the S1 to the secondary somatosensory cortex (S2). The parallel processing theory suggests that tactile information is directly transmitted from the thalamusto both the S1 and S2. In both non-primate and lower primate mammals, tactile so-matosensory information is processed in parallel in the network between thalamus and somato-sensory cortices. However, the processing of tactile somatosensory information in higher primates and humans remains, at present, a matter of debate. Indeed, the results of previous studies are somehow contradicting, which could be due to some inherent limitations: including stimulus pat-terns, data collection techniques, and data analysis methods. Under the current technical conditions, future research should rely more on experimental design to explore the top-down influence and brain plasticity on the processing of tactile information to further investigate the underlying neural mechanisms.

文章引用: 武广起 , 夏晓磊 , 胡 理 (2016) 串行处理还是并行处理?触觉信息在丘脑–体感皮层网络上的加工方式。 心理学进展, 6, 890-899. doi: 10.12677/AP.2016.68114

参考文献

[1] Hagiwara, K., Okamoto, T., Shigeto, H., Ogata, K., Somehara, Y., Matsushita, T., Tobimatsu, S. et al. (2010). Oscillatory Gamma Synchronization Binds the Primary and Secondary Soma-tosensory Areas in Humans. Neuroimage, 51, 412-420.
http://dx.doi.org/10.1016/j.neuroimage.2010.02.001

[2] Ahlfors, S. P., Han, J., Belliveau, J. W., & Hämäläinen, M. S. (2010). Sensitivity of MEG and EEG to Source Orientation. Brain Topography, 23, 227-232.
http://dx.doi.org/10.1007/s10548-010-0154-x

[3] Blatow, M., Nennig, E., Durst, A., Sartor, K., & Stippich, C. (2007). fMRI Reflects Functional Connectivity of Human Somatosensory Cortex. Neuroimage, 37, 927-936.
http://dx.doi.org/10.1016/j.neuroimage.2007.05.038

[4] Hall, E. L., Robson, S. E., Morris, P. G., & Brookes, M. J. (2014). The relationship between MEG and fMRI. Neuroimage, 102, 80-91.
http://dx.doi.org/10.1016/j.neuroimage.2013.11.005

[5] Hu, L., Zhang, Z. G., & Hu, Y. (2012). A Time-Varying Source Connectivity Approach to Reveal Human Somatosensory Information Processing. Neuroimage, 62, 217-228.
http://dx.doi.org/10.1016/j.neuroimage.2012.03.094

[6] Inui, K., Wang, X., Tamura, Y., Kaneoke, Y., & Kakigi, R. (2004). Serial Processing in the Human Somatosensory System. Cerebral Cortex, 14, 851-857.
http://dx.doi.org/10.1093/cercor/bhh043

[7] Burton, H., Fabri, M., & Alloway, K. (1995). Cortical Areas within the Lateral Sulcus Connected to Cutaneous Representations in Areas 3b and 1: A Revised Interpretation of the Second Somatosensory Area in Macaque Monkeys. Journal of Comparative Neurology, 355, 539-562.
http://dx.doi.org/10.1002/cne.903550405

[8] Johansson, R. S., & Flanagan, J. R. (2009). Coding and Use of Tactile Signals from the Fingertips in Object Manipulation Tasks. Nature Reviews Neuroscience, 10, 345-359.
http://dx.doi.org/10.1038/nrn2621

[9] Chen, T. L., Babiloni, C., Ferretti, A., Perrucci, M. G., Romani, G. L., Rossini, P. M., Tartaro, A., & Del Gratta, C. (2008). Human Secondary Somatosensory Cortex Is Involved in the Processing of Somatosensory Rare Stimuli: An fMRI Study. Neuroimage, 40, 1765-1771.
http://dx.doi.org/10.1016/j.neuroimage.2008.01.020

[10] Kalberlah, C., Villringer, A., & Pleger, B. (2013). Dynamic Causal Modeling Suggests Serial Processing of Tactile Vibratory Stimuli in the Human Somatosensory Cortex—An fMRI Study. Neuroi-mage, 74, 164-171.
http://dx.doi.org/10.1016/j.neuroimage.2013.02.018

[11] Chung, Y. G., Han, S. W., Kim, H.-S., Chung, S.-C., Park, J.-Y., Wallraven, C., & Kim, S.-P. (2014). Intra- and Inter- Hemispheric Effective Connectivity in the Human Somato-sensory Cortex during Pressure Stimulation. BMC Neuroscience, 15, 43.
http://dx.doi.org/10.1186/1471-2202-15-43

[12] Chung, Y. G., Kim, J., Han, S. W., Kim, H.-S., Choi, M. H., Chung, S.-C., Park, J. Y., & Kim, S.-P. (2013). Frequency- Dependent Patterns of Somatosensory Cortical Responses to Vibro-tactile Stimulation in Humans: A fMRI Study. Brain Research, 1504, 47-57.
http://dx.doi.org/10.1016/j.brainres.2013.02.003

[13] Delmas, P., Hao, J., & Rodat-Despoix, L. (2011). Molecular Mechanisms of Mechanotransduction in Mammalian Sensory Neurons. Nature Reviews Neuroscience, 12, 139-153.
http://dx.doi.org/10.1038/nrn2993

[14] Engel, A. K., Fries, P., & Singer, W. (2001). Dynamic Predictions: Oscillations and Synchrony in Top-Down Processing. Nature Reviews Neuroscience, 2, 704-716.
http://dx.doi.org/10.1038/35094565

[15] Karhu, J., & Tesche, C. D. (1999). Simultaneous Early Processing of Sensory Input in Human Primary (SI) and Secondary (SII) Somatosensory Cortices. Journal of Neurophysi-ology, 81, 2017-2025.

[16] Khoshnejad, M., Piché, M., Saleh, S., Duncan, G., & Rainville, P. (2014). Serial Processing in Primary and Secondary Somatosensory Cortex: A DCM Analysis of Human fMRI Data in Response to Innocuous and Noxious Electrical Stimulation. Neuroscience Letters, 577, 83-88.
http://dx.doi.org/10.1016/j.neulet.2014.06.013

[17] Fitzgerald, P. J., Lane, J. W., Thakur, P. H., & Hsiao, S. S. (2006). Receptive Field (RF) Properties of the Macaque Second Somatosensory Cortex: RF Size, Shape, and Somatotopic Organization. The Journal of Neuroscience, 26, 6485-6495.
http://dx.doi.org/10.1523/JNEUROSCI.5061-05.2006

[18] Klingner, C. M., Brodoehl, S., Huonker, R., Götz, T., Baumann, L., & Witte, O. W. (2015). Parallel Processing of Somatosensory Information: Evidence from Dynamic Causal Modeling of MEG Data. Neuroimage, 118, 193-198.
http://dx.doi.org/10.1016/j.neuroimage.2015.06.028

[19] Friedman, D. P., & Murray, E. A. (1986). Thalamic Connectivity of the Second Somatosensory Area and Neighboring Somatosensory Fields of the Lateral Sulcus of the Ma-caque. Journal of Comparative Neurology, 252, 348-373.
http://dx.doi.org/10.1002/cne.902520305

[20] Knecht, S., Kunesch, E., & Schnitzler, A. (1996). Parallel and Serial Processing of Haptic Information in Man: Effects of Parietal Lesions on Sensorimotor Hand Function. Neurop-sychologia, 34, 669-687.
http://dx.doi.org/10.1016/0028-3932(95)00148-4

[21] Friedman, R. M., Chen, L. M., & Roe, A. W. (2004). Modality Maps within Primate Somatosensory Cortex. Proceedings of the National Academy of Sciences of the United States of America, 101, 12724-12729.
http://dx.doi.org/10.1073/pnas.0404884101

[22] Friston, K. (2005). A Theory of Cortical Responses. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 360, 815-836.
http://dx.doi.org/10.1098/rstb.2005.1622

[23] Koch, S. P., Habermehl, C., Mehnert, J., Schmitz, C. H., Holtze, S., Villringer, A., Obrig, H. et al. (2010). High-Resolution Optical Functional Mapping of the Human Somatosensory Cortex. Frontiers in Neuroenergetics, 2, 12.
http://dx.doi.org/10.3389/fnene.2010.00012

[24] Frot, M., Magnin, M., Mauguière, F., & Garcia-Larrea, L. (2007). Human SII and Posterior Insula Differently Encode Thermal Laser Stimuli. Cerebral Cortex, 17, 610-620.
http://dx.doi.org/10.1093/cercor/bhk007

[25] Gao, L., Sommerlade, L., Coffman, B., Zhang, T. S., Stephen, J. M., Li, D. C., Wang, J., Grebogi, C., & Schelter, B. (2015). Granger Causal Time-Dependent Source Connectivity in the Somato-sensory Network. Scientific Reports, 5.
http://dx.doi.org/10.1038/srep10399

[26] Kolb, B., & Whishaw, I. Q. (1998). Brain Plasticity and Behavior. Annual Review of Psychology, 49, 43-64.
http://dx.doi.org/10.1146/annurev.psych.49.1.43

[27] Garraghty, P. E., Florence, S. L., Tenhula, W. N., & Kaas, J. H. (1991). Parallel Thalamic Activation of the First and Second Somatosensory Areas in Prosimian Primates and Tree Shrews. Journal of Comparative Neurology, 311, 289-299.
http://dx.doi.org/10.1002/cne.903110209

[28] Krubitzer, L. A., & Kaas, J. H. (1992). The Somatosensory Thalamus of Monkeys: Cortical Connections and a Redefinition of Nuclei in Marmosets. Journal of Comparative Neurology, 319, 123-140.
http://dx.doi.org/10.1002/cne.903190111

[29] Garraghty, P. E., Pons, T. P., & Kaas, J. H. (1990). Ablations of Areas 3b (SI Proper) and 3a of Somatosensory Cortex in Marmosets Deactivate the Second and Parietal Ventral Somatosensory Areas. Somatosensory & Motor Research, 7, 125- 135.
http://dx.doi.org/10.3109/08990229009144703

[30] Gilbert, C. D., & Li, W. (2013). Top-Down Influences on Visual Processing. Nature Reviews Neuroscience, 14, 350-363.
http://dx.doi.org/10.1038/nrn3476

[31] Liang, M., Mouraux, A., & Iannetti, G. D. (2011). Parallel Processing of Nociceptive and Non-Nociceptive Somatosensory Information in the Human Primary and Secondary Somatosensory Cortices: Evidence from Dynamic Causal Modeling of Functional Magnetic Resonance Imaging Data. The Journal of Neuroscience, 31, 8976-8985.
http://dx.doi.org/10.1523/JNEUROSCI.6207-10.2011

[32] Gilbert, C. D., & Sigman, M. (2007). Brain States: Top-Down Influences in Sensory Processing. Neuron, 54, 677-696.
http://dx.doi.org/10.1016/j.neuron.2007.05.019

[33] Lin, Y. Y., & Forss, N. (2002). Functional Characteriza-tion of Human Second Somatosensory Cortex by Magnetoencephalography. Behavioural Brain Research, 135, 141-145.
http://dx.doi.org/10.1016/S0166-4328(02)00143-2

[34] Lockwood, P. L., Iannetti, G. D., & Haggard, P. (2013). Transcranial Magnetic Stimulation over Human Secondary Somatosensory Cortex Disrupts Perception of Pain Intensity. Cortex, 49, 2201-2209.
http://dx.doi.org/10.1016/j.cortex.2012.10.006

[35] Logothetis, N. K. (2008). What We Can Do and What We Cannot Do with fMRI. Nature, 453, 869-878.
http://dx.doi.org/10.1038/nature06976

[36] McGlone, F., & Reilly, D. (2010). The Cutaneous Sensory System. Neu-roscience & Biobehavioral Reviews, 34, 148-159.
http://dx.doi.org/10.1016/j.neubiorev.2009.08.004

[37] Murray, G. M., Zhang, H. Q., Kaye, A. N., Sinnadurai, T., Campbell, D. H., & Rowe, M. J. (1992). Parallel Processing in Rabbit First (SI) and Second (SII) Somatosensory Cortical Areas: Effects of Reversible Inactivation by Cooling of SI on Responses in SII. Journal of Neurophysiology, 68, 703-710.

[38] Onishi, H., Oyama, M., Soma, T., Kubo, M., Kirimoto, H., Murakami, H., & Kameyama, S. (2010). Neu-romagnetic Activation of Primary and Secondary Somatosensory Cortex Following Tactile-On and Tactile-Off Stimulation. Clinical Neurophysiology, 121, 588-593.
http://dx.doi.org/10.1016/j.clinph.2009.12.022

[39] Pais-Vieira, M., Lebedev, M. A., Wiest, M. C., & Nicolelis, M. A. L. (2013). Simultaneous Top-Down Modulation of the Primary Somatosensory Cortex and Thalamic Nuclei during Active Tactile Discrimination. Journal of Neuroscience, 33, 4076-4093.
http://dx.doi.org/10.1523/JNEUROSCI.1659-12.2013

[40] Pascual-Leone, A., Amedi, A., Fregni, F., & Merabet, L. B. (2005). The Plastic Human Brain Cortex. Annual Review of Neuroscience, 28, 377-401.
http://dx.doi.org/10.1146/annurev.neuro.27.070203.144216

[41] Ploner, M., Gross, J., Timmermann, L., & Schnitzler, A. (2006). Pain Processing Is Faster than Tactile Processing in the Human Brain. The Journal of Neuroscience, 26, 10879-10882.
http://dx.doi.org/10.1523/JNEUROSCI.2386-06.2006

[42] Ploner, M., Schoffelen, J.-M., Schnitzler, A., & Gross, J. (2009). Functional Integration within the Human Pain System as Revealed by Granger Causality. Human Brain Mapping, 30, 4025-4032.
http://dx.doi.org/10.1002/hbm.20826

[43] Pons, T. P., & Kaas, J. H. (1986). Corti-cocortical Connections of Area 2 of Somatosensory Cortex in Macaque Monkeys: A Correlative Anatomical and Electro-physiological Study. Journal of Comparative Neurology, 248, 313-335.
http://dx.doi.org/10.1002/cne.902480303

[44] Pons, T. P., Garraghty, P. E., & Mishkin, M. (1992). Serial and Parallel Processing of Tactual Information in Somatosensory Cortex of Rhesus Monkeys. Journal of Neurophysiology, 68, 518-527.

[45] Raij, T., Karhu, J., Kičić, D., Lioumis, P., Julkunen, P., Lin, F.-H., Hämäläinen, M. et al. (2008). Parallel Input Makes the Brain Run Faster. Neuroimage, 40, 1792-1797.
http://dx.doi.org/10.1016/j.neuroimage.2008.01.055

[46] Ramalingam, N., McManus, J. N. J., Li, W., & Gilbert, C. D. (2013). Top-Down Modulation of Lateral Interactions in Visual Cortex. The Journal of Neuroscience, 33, 1773-1789.
http://dx.doi.org/10.1523/JNEUROSCI.3825-12.2013

[47] Rowe, M. J., Turman, A. B., Murray, G. M., & Zhang, H. Q. (1996). Parallel Organization of Somatosensory Cortical Areas I and II for Tactile Processing. Clinical and Experimental Pharmacology and Physiology, 23, 931-938.
http://dx.doi.org/10.1111/j.1440-1681.1996.tb01145.x

[48] Sale, A., Berardi, N., & Maffei, L. (2014). Environment and Brain Plasticity: Towards an Endogenous Pharmacotherapy. Physiological Reviews, 94, 189-234.
http://dx.doi.org/10.1152/physrev.00036.2012

[49] Schnitzler, A., & Ploner, M. (2000). Neurophysiology and Func-tional Neuroanatomy of Pain Perception. Journal of Clinical Neurophysiology, 17, 592-603.
http://dx.doi.org/10.1097/00004691-200011000-00005

[50] Thakur, P. H., Fitzgerald, P. J., Lane, J. W., & Hsiao, S. S. (2006). Receptive Field Properties of the Macaque Second Somatosensory Cortex: Nonlinear Mechanisms Underlying the Representation of Orientation within a Finger Pad. The Journal of Neuroscience, 26, 13567-13575.
http://dx.doi.org/10.1523/JNEUROSCI.3990-06.2006

[51] Treede, R.-D., Kenshalo, D. R., Gracely, R. H., & Jones, A. K. P. (1999). The Cortical Representation of Pain. Pain, 79, 105-111.
http://dx.doi.org/10.1016/S0304-3959(98)00184-5

[52] Turman, A. B., Ferrington, D. G., Ghosh, S., Morley, J. W., & Rowe, M. J. (1992). Parallel Processing of Tactile Information in the Cerebral Cortex of the Cat: Effect of Reversible Inactivation of SI on Responsiveness of SII Neurons. Journal of Neurophysiology, 67, 411-429.

[53] Valdes-Sosa, P. A., Roebroeck, A., Daunizeau, J., & Friston, K. (2011). Effective Connectivity: Influence, Causality and Biophysical Modeling. Neuroimage, 58, 339-361.
http://dx.doi.org/10.1016/j.neuroimage.2011.03.058

[54] Wasaka, T., Nakata, H., Akatsuka, K., Kida, T., Inui, K., & Kakigi, R. (2005). Differential Modulation in Human Primary and Secondary Somatosensory Cortices during the Preparatory Period of Self-Initiated Finger Movement. European Journal of Neuroscience, 22, 1239-1247.
http://dx.doi.org/10.1111/j.1460-9568.2005.04289.x

[55] Worthen, S. F., Hobson, A. R., Hall, S. D., Aziz, Q., & Furlong, P. L. (2011). Primary and Secondary Somatosensory Cortex Responses to Anticipation and Pain: A Magnetoencephalography Study. European Journal of Neuroscience, 33, 946-959.
http://dx.doi.org/10.1111/j.1460-9568.2010.07575.x

[56] Zhang, H. Q., Murray, G. M., Coleman, G. T., Turman, A. B., Zhang, S. P., & Rowe, M. J. (2001). Functional Characteristics of the Parallel SI-and SII-Projecting Neurons of the Thalamic Ventral Posterior Nucleus in the Marmoset. Journal of Neurophysiology, 85, 1805-1822.

[57] Zhang, H. Q., Murray, G. M., Turman, A. B., Mackie, P. D., Coleman, G. T., & Rowe, M. J. (1996). Parallel Processing in Cerebral Cortex of the Marmoset Monkey: Effect of Reversible SI Inactivation on Tactile Responses in SII. Journal of Neurophysi-ology, 76, 3633-3655.

[58] Zhang, H. Q., Zachariah, M. K., Coleman, G. T., & Rowe, M. J. (2001). Hierarchical Equi-valence of Somatosensory Areas I and II for Tactile Processing in the Cerebral Cortex of the Marmoset Monkey. Journal of Neurophysiology, 85, 1823- 1835.

[59] Grabenhorst, F., & Rolls, E. T. (2010). Attentional Modulation of Affective versus Sensory Processing: Functional Connectivity and a Top-Down Biased Activation Theory of Selective Attention. Journal of Neurophysiology, 104, 1649-1660.
http://dx.doi.org/10.1152/jn.00352.2010

[60] Zhang, N., Gore, J. C., Chen, L. M., & Avison, M. J. (2007). Dependence of BOLD Signal Change on Tactile Stimulus Intensity in SI of Primates. Magnetic Resonance Imaging, 25, 784-794.
http://dx.doi.org/10.1016/j.mri.2007.05.002

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