Exclusive:Sensory Integration and Its Brain Mechanisms

Neural mechanisms of tactile information processing

  • ZHOU Lili, YAO Xinru, TANG Zhengyu, REN Qiaoyue, LÜ Xuejing, HU Li
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  • 1. Key Laboratory of Mental Health;Institute of Psychology, Chinese Academy of Sciences, Beijing 100101, China;
    2. Department of Psychology, University of Chinese Academy of Sciences, Beijing 100049, China

Received date: 2017-05-31

  Revised date: 2017-08-24

  Online published: 2017-10-18

Abstract

To perceive external environment more efficiently, the sensory information derived from the modality of touch, or tactile information, is processed in terms of its physical features and affective responses to these features. This review summarizes the current understanding about how haptic information is processed in skin, spinal cord, and cerebral cortex of animals and humans. Typically, different non-noxious somatosensory information is coded by various cutaneous sensory neurons called low-threshold mechanoreceptors (LTMRs). Next, haptic processing starts at the dorsal horn of the spinal cord, and then it partially segregates into different pathways, transmitting information to the somatosensory cortex, the first crucial brain area for haptic information processing. Moreover, several relatively independent brain networks are responsible for the processing of different properties of haptic information. Finally, by discussing the interactions between touch and other sensory modalities, we argue that such interactions are plastic, which is warranted in the future work to generate extensive value in applications.

Cite this article

ZHOU Lili, YAO Xinru, TANG Zhengyu, REN Qiaoyue, LÜ Xuejing, HU Li . Neural mechanisms of tactile information processing[J]. Science & Technology Review, 2017 , 35(19) : 37 -43 . DOI: 10.3981/j.issn.1000-7857.2017.19.004

References

[1] Stilla R, Sathian K. Selective visuo-haptic processing of shape and tex-ture[J]. Human Brain Mapping, 2008, 29(10):1123-1138.
[2] Hertenstein M J, Keltner D, App B, Bulleit B A, Jaskolka A R. Touch communicates distinct emotions[J]. Emotion, 2006, 6(3):528-533.
[3] McGlone F, Wessberg J, Olausson H. Discriminative and affective touch:sensing and feeling[J]. Neuron, 2014, 82(4):737-755.
[4] Griffin J W, McArthur J C, Polydefkis M. Assessment of cutaneous in-nervation by skin biopsies[J]. Current Opinion in Neurology, 2001, 14(5):655-659.
[5] Abraira V E, Ginty D D. The sensory neurons of touch[J]. Neuron, 2013, 79(4):618-639.
[6] Sathian K. Analysis of haptic information in the cerebral cortex[J]. Jour-nal of Neurophysiology, 2016, 116(4):1795-1806.
[7] Kim S S, Gomez-Ramirez M, Thakur P H, et al. Multimodal interac-tions between proprioceptive and cutaneous signals in primary somato-sensory cortex[J]. Neuron, 2015, 86:555-566.
[8] Yau J M, Pasupathy A, Fitzgerald P J, Hsiao S S, Connor C E. Analo-gous intermediate shape coding in vision and touch[J]. PNAS, 2009, 106(38):16457-16462.
[9] Stoesz M R, Zhang M, Weisser V D, et al. Sathian K. Neural networks active during tactile form perception:common and differential activity during macrospatial and microspatial tasks[J]. International Journal of Psychophysiology, 2003, 50(1):41-49.
[10] Stilla R, Deshpande G, LaConte S, et al. Posteromedial parietal corti-cal activity and inputs predict tactile spatial acuity[J]. Journal of Neu-roscience, 2007, 27:11091-11102.
[11] Freides D. Human information processing and sensory modality:Crossmodal functions, information complexity, memory, and deficit[J]. Psy-chological Bulletin, 1974, 81(5):284-310.
[12] Ernst M O, Bülthoff H H. Merging the senses into a robust percept[J]. Trends in Cognitive Sciences, 2004, 8(4):162-169.
[13] Foxe J J, Schroeder C E. The case for feedforward multisensory conver-gence during early cortical processing[J]. Neuroreport, 2005, 16(5):419-423.
[14] Bryan R N, Trevino D L, Coulter J D, et al. Location and somatotopic organization of the cells of origin of the spino-cervical tract[J]. Experi-mental Brain Research, 1973. 17(2):177-189.
[15] Björnsdotter M, Löken L, Olausson H, et al. Somatotopic organization of gentle touch processing in the posterior insular cortex[J]. Journal of Neuroscience, 2009. 29(29):9314-9320.
[16] Löken L S, Wessberg J, Morrison I, et al. Coding of pleasant touch by unmyelinated afferents in humans[J]. Nature Neuroscience, 2009, 12(5):547-548.
[17] Williams A L. Skin relaxation predicts neural firing rate adaptation in sai touch receptors[C]//2010 Annual International Conference of the IEEE Engineering in Medicine and Biology Society. Buenos Aires, Ar-gentina:Conference Proceedings IEEE Engineering in Medicine and Biology Society, 2010:6678-6681.
[18] Ikeda I, Yamashita Y, Ono T, et al. Selective phototoxic destruction of rat Merkel cells abolishes responses of slowly adapting type I mecha-noreceptor units[J]. Journal of Physiology, 1994, 479(Pt 2):247-256.
[19] Maricich S M, et al. Merkel cells are essential for light-touch respons-es[J]. Science, 2009, 324(5934):1580-1582.
[20] Rahman F, et al. Detection of acid-sensing ion channel 3(ASIC3) in periodontal Ruffini endings of mouse incisors[J]. Neuroscience Letters, 2011, 488(2):173-177.
[21] Goodwin A W, Macefield V G, Bisley J W. Encoding of object curva-ture by tactile afferents from human fingers[J]. Journal of Neurophysi-ology, 1997, 78(6):2881-2888.
[22] Blake D T, Hsiao S S, Johnson K O. Neural coding mechanisms in tac-tile pattern recognition:The relative contributions of slowly and rapid-ly adapting mechanoreceptors to perceived roughness[J]. Journal of Neuroscience, 1997, 17(19):7480-7489.
[23] Paré M, Elde R, Mazurkiewicz J E, et al. The Meissner corpuscle re-vised:a multiafferented mechanoreceptor with nociceptor immuno-chemical properties[J]. Journal of Neuroscience, 2001, 21(18):7236-7246.
[24] Lynn B. The form and distribution of the receptive fields of Pacinian corpuscles found in and around the cat's large foot pad[J]. Journal of Physiology, 1971, 217(3):755-771.
[25] Bell J, Bolanowski S, Holmes M H. The structure and function of Pa-cinian corpuscles:A review[J]. Progress in Neurobiology, 1994, 42(1):79-128.
[26] Ackerley R, Wasling H B, Liljencrantz J, et al. Human C-tactile affer-ents are tuned to the temperature of a skin-stroking caress[J]. Journal of Neuroscience, 2014, 34(8):2879-2883.
[27] Kumazawa T, Perl E R. Primate cutaneous sensory units with unmy-elinated (C) afferent fibers[J]. Journal of Neurophysiology, 1977, 40(6):1325-1338.
[28] Jörntell H, Bengtsson F, Geborek P, et al. Segregation of tactile input features in neurons of the cuneate nucleus[J]. Neuron, 2014, 83(6):1444-1452.
[29] Giesler G J, Nahin R L, Madsen A M. Postsynaptic dorsal column pathway of the rat. I. Anatomical studies[J]. Journal of Neurophysiolo-gy, 1984, 51(2):260-275.
[30] Taub A, Bishop P O. The spinocervical tract:Dorsal column linkage, conduction velocity, primary afferent spectrum[J]. Experimental Neu-rology, 1965, 13(1):1-21.
[31] Li L, Rutlin M, Abraira V E, Cassidy C, et al. The functional organiza-tion of cutaneous low-threshold mechanosensory neurons[J]. Cell, 2011, 147(7):1615-1627.
[32] Hu L, Zhang Z G, Hu Y. A time-varying source connectivity ap-proach to reveal human somatosensory information processing[J]. Neu-roimage, 2012, 62(1):217-228.
[33] Gallace A, Spence C. Touch and the body:The role of the somatosen-sory cortex in tactile awareness[J]. Psyche:An Interdisciplinary Jour-nal of Research on Consciousness, 2010, 16(1):31-67.
[34] 武广起, 夏晓磊, 胡理. 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[J]. 心理学进展, 2016, 6(8):890-899. Wu Guangqi, Xia Xiaolei, Hu Li. Serial or parallel processing? The processing of tactile information in the network between thalamus and somatosensory cortices[J]. Advances in Psychology, 2016, 6(8):890-899.
[35] O'Sullivan B T, Roland P E, Kawashima R. A PET study of somato-sensory discrimination in man. Microgeometry versus microgeometry[J]. European Journal of Neuroscience, 1994, 6(1):137-148.
[36] Ledberg A, O'Sullivan B T, Kinomura S, et al. Somatosensory activa-tions of the parietal operculum of man. A PET study[J]. European Journal of Neuroscience. 1995, 7(9):1934-1941.
[37] Lederman S, Gati J, Servos P, et al. fMRI-derived cortical maps for haptic shape, texture, and hardness[J]. Cognitive Brain Research, 2001, 12(2):307-313.
[38] Sathian K, Lacey S, Stilla R, et al. Dual pathways for haptic and visu-al perception of spatial and texture information[J]. Neuroimage, 2011, 57(2):462-475.
[39] Stilla R, Sathian K. Selective visuo-haptic processing of shape and texture[J]. Human Brain Mapping, 2008, 29(10):1123-1138.
[40] Eck J, Kaas A L, Goebel R. Crossmodal interactions of haptic and vi-sual texture information in early sensory cortex[J]. Neuroimage, 2013, 75:123-135.
[41] Hegner Y L, Lee Y, Grodd W, Braun C. Comparing tactile pattern and vibrotactile frequency discrimination:a human FMRI study[J]. Journal of Neurophysiology, 2010, 103(6):3115-3122.
[42] Sathian K. Analysis of haptic information in the cerebral cortex[J]. Journal of Neurophysiology, 2016, 116(4):1795-1806.
[43] Deshpande G, Hu X, Stilla R, et al. Effective connectivity during hap-tic perception:a study using granger causality analysis of functional magnetic resonance imaging data[J]. Neuroimage, 2008, 40(4), 1807-1814.
[44] Kim S S, Gomez-Ramirez M, Thakur P, et al. Multimodal interactions between proprioceptive and cutaneous signals in primary somatosenso-ry cortex[J]. Neuron, 2015, 86(2), 555-566.
[45] Olausson H, Lamarre Y, Backlund H, et al. Unmyelinated tactile affer-ents signal touch and project to insular cortex[J]. Nature Neurosci-ence, 2002, 5(9):900-904.
[46] Kostovic I, Judas M. The development of the subplate and thalamocor-tical connections in the human foetal brain[J]. Acta Paediatrica, 2010, 99(8):1119-1127.
[47] Gordon I, Voos A C, Bennett R H, et al. Brain mechanisms for pro-cessing affective touch[J]. Human Brain Mapping, 2013, 34(4):914-922.
[48] Chen J I, Ha B, Bushnell M C, et al. Differentiating noxious-and in-nocuous-related activation of human somatosensory cortices using tem-poral analysis of fMRI[J]. Journal of Neurophysiology, 2002, 88(1):464-474.
[49] Fabrizi L, Slater R, Worley A, et al. A shift in sensory processing that enables the developing human brain to discriminate touch from pain[J]. Current Biology, 2011, 21(18):1552-1558.
[50] Vance C, Dailey D, Rakel B, et al. A novel method to obtain higher intensity TENS stimulation in clinical application[J]. Journal of Pain, 2015, 16(4):S93-S93.
[51] Melzack R, Wall P D. Pain mechanisms:New theory[J]. Science, 1965, 150(3699):971-979.
[52] Hayamizu M, Hagiwara K, Hironaga N, et al. A spatiotemporal signa-ture of cortical pain relief by tactile stimulation:An MEG study[J]. Neuroimage, 2016, 130:175-83.
[53] Jensen T S, Finnerup N B. Allodynia and hyperalgesia in neuropathic pain:clinical manifestations and mechanisms[J]. The Lancet Neurolo-gy, 2014, 13(9):924-935.
[54] Chang P C, Centeno M V, Procissi D, et al. Brain activity for tactile allodynia:a longitudinal awake rat functional magnetic resonance im-aging study tracking emergence of neuropathic pain[J]. Pain, 2017, 158(3):488-497.
[55] Macaluso E, Maravita A. The representation of space near the body through touch and vision[J]. Neuropsychologia, 2010, 48(3):782-795.
[56] Ward J, Banissy M J. Explaining mirror-touch synesthesia[J]. Cogni-tive Neuroscience, 2015, 6(2-3):118-133.
[57] Collins K L, Guterstam A, Cronin J, et al. Ownership of an artificial limb induced by electrical brain stimulation[J]. PNAS, 2016, 114(1):166-171.
[58] Nordmark P F, Pruszynski J A, Johansson R S. BOLD responses to tactile stimuli in visual and auditory cortex depend on the frequency content of stimulation[J]. Journal of Cognitive Neuroscience, 2012, 24(10):2120-2134.
[59] Van W D, Lätt J, Englund E, et al. Tumor extension in high-grade gli-omas assessed with diffusion magnetic resonance imaging:values and lesion-to-brain ratios of apparent diffusion coefficient and fractional anisotropy[J]. Acta Radiologica, 2006, 47(3):311-319.
[60] Manfredi L R, Saal H P, Brown K J, et al. Natural scenes in tactile texture[J]. Journal of Neurophysiology, 2014, 111(9):1792-1802.
[61] Crommett L E, Pérezbellido A, Yau J M. Auditory adaptation im-proves tactile frequency perception[J]. Journal of Neurophysiology, 2017, 117(3):1352-1362.
[62] Tonelli A, Gori M, Brayda L. The influence of tactile cognitive maps on auditory space perception in sighted persons[J]. Frontiers in Psy-chology, 2016, 7:1683.
[63] Schürmann M, Caetano G, Hlushchuk Y, et al. Touch activates human auditory cortex[J]. Neuroimage, 2006, 30(4):1325-1331.
[64] Ro T, Farnè A, Johnson R M, et al. Feeling sounds after a thalamic le-sion[J]. Annals of Neurology, 2007, 62(5):433-441.
[65] Rutkowski T M, Mori H. Tactile and bone-conduction auditory brain computer interface for vision and hearing impaired users[J]. Journal of Neuroscience Methods, 2015, 244:45-51.
[66] Dawson G, Watling R. Interventions to facilitate auditory, visual, and motor integration in autism:A review of the evidence[J]. Journal of Au-tism and Developmental Disorders, 2000, 30(5):415-421.
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