Somatotopic Organization of Gentle Touch Processing in the Posterior Insular Cortex

A network of thin (C and Aδ) afferents relays various signals related to the physiological condition of the body, including sensations of gentle touch, pain, and temperature changes. Such afferents project to the insular cortex, where a somatotopic organization of responses to noxious and cooling stimuli was recently observed. To explore the possibility of a corresponding body-map topography in relation to gentle touch mediated through C tactile (CT) fibers, we applied soft brush stimuli to the right forearm and thigh of a patient (GL) lacking Aβ afferents, and six healthy subjects during functional magnetic resonance imaging (fMRI). For improved fMRI analysis, we used a highly sensitive multivariate voxel clustering approach. A somatotopic organization of the left (contralateral) posterior insular cortex was consistently demonstrated in all subjects, including GL, with forearm projecting anterior to thigh stimulation. Also, despite denying any sense of touch in daily life, GL correctly localized 97% of the stimuli to the forearm or thigh in a forced-choice paradigm. The consistency in activation patterns across GL and the healthy subjects suggests that the identified organization reflects the central projection of CT fibers. Moreover, substantial similarities of the presently observed insular activation with that described for noxious and cooling stimuli solidify the hypothesized sensory-affective role of the CT system in the maintenance of physical well-being as part of a thin-afferent homeostatic network.

[1]  Y. Lamarre,et al.  Postural adjustments associated with different unloadings of the forearm: effects of proprioceptive and cutaneous afferent deprivation. , 1995, Canadian journal of physiology and pharmacology.

[2]  Johan Wessberg,et al.  Unmyelinated tactile afferents have opposite effects on insular and somatosensory cortical processing , 2008, Neuroscience Letters.

[3]  Y. Zotterman Touch, pain and tickling: an electro‐physiological investigation on cutaneous sensory nerves , 1939, The Journal of physiology.

[4]  A. Craig How do you feel? Interoception: the sense of the physiological condition of the body , 2002, Nature Reviews Neuroscience.

[5]  Jonathan C. W. Brooks,et al.  Somatotopic organisation of the human insula to painful heat studied with high resolution functional imaging , 2005, NeuroImage.

[6]  J. Wessberg,et al.  Coding of pleasant touch by unmyelinated afferents in humans , 2009, Nature Neuroscience.

[7]  H. Harlow The Nature of Love , 1958 .

[8]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[9]  Terry M. Peters,et al.  3D statistical neuroanatomical models from 305 MRI volumes , 1993, 1993 IEEE Conference Record Nuclear Science Symposium and Medical Imaging Conference.

[10]  J. Price,et al.  Brain mediation of active and passive emotional coping. , 2000, Progress in brain research.

[11]  U. Norrsell,et al.  Spatial cues serving the tactile directional sensibility of the human forearm. , 1994, The Journal of physiology.

[12]  J. Haynes Brain Reading: Decoding Mental States From Brain Activity In Humans , 2011 .

[13]  T. Jessell PAIN , 1982, The Lancet.

[14]  A. Craig,et al.  Nociceptive and thermoreceptive lamina I neurons are anatomically distinct , 1998, Nature Neuroscience.

[15]  Johan Wessberg,et al.  Discriminative touch and emotional touch. , 2007, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[16]  S. Siegel,et al.  Nonparametric Statistics for the Behavioral Sciences , 2022, The SAGE Encyclopedia of Research Design.

[17]  A. Craig,et al.  Is neuropathic pain caused by the activation of nociceptive‐specific neurons due to anatomic sprouting in the dorsal horn? , 2000, The Journal of comparative neurology.

[18]  M. Bushnell,et al.  A thalamic nucleus specific for pain and temperature sensation , 1994, Nature.

[19]  A. R. Muir,et al.  The structure and function of a slowly adapting touch corpuscle in hairy skin , 1969, The Journal of physiology.

[20]  A. Craig,et al.  Pain mechanisms: labeled lines versus convergence in central processing. , 2003, Annual review of neuroscience.

[21]  E. Perl,et al.  Central projections of identified, unmyelinated (C) afferent fibers innervating mammalian skin. , 1986, Science.

[22]  T. Naidich,et al.  The insula: anatomic study and MR imaging display at 1.5 T. , 2004, AJNR. American journal of neuroradiology.

[23]  David D. Cox,et al.  Functional magnetic resonance imaging (fMRI) “brain reading”: detecting and classifying distributed patterns of fMRI activity in human visual cortex , 2003, NeuroImage.

[24]  Sterling C. Johnson,et al.  Anteroposterior somatotopy of innocuous cooling activation focus in human dorsal posterior insular cortex. , 2005, American journal of physiology. Regulatory, integrative and comparative physiology.

[25]  S. C. Gandevia,et al.  Somatotopic organization of the processing of muscle and cutaneous pain in the left and right insula cortex: A single-trial fMRI study , 2007, Pain.

[26]  E. Perl,et al.  Primate cutaneous sensory units with unmyelinated (C) afferent fibers. , 1977, Journal of neurophysiology.

[27]  M Nordin,et al.  Low‐threshold mechanoreceptive and nociceptive units with unmyelinated (C) fibres in the human supraorbital nerve. , 1990, The Journal of physiology.

[28]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[29]  J. Wessberg,et al.  Functional role of unmyelinated tactile afferents in human hairy skin: sympathetic response and perceptual localization , 2007, Experimental Brain Research.

[30]  Y. Lamarre,et al.  Unmyelinated tactile afferents signal touch and project to insular cortex , 2002, Nature Neuroscience.

[31]  P R Burgess,et al.  Dynamic properties of mechanoreceptors with unmyelinated (C) fibers. , 1971, Journal of neurophysiology.

[32]  J. Wessberg,et al.  Unmyelinated afferents constitute a second system coding tactile stimuli of the human hairy skin. , 1999, Journal of neurophysiology.

[33]  R. Shah,et al.  Least Squares Support Vector Machines , 2022 .

[34]  Tom M. Mitchell,et al.  Learning to Decode Cognitive States from Brain Images , 2004, Machine Learning.

[35]  Johan Wessberg,et al.  An Evolutionary Approach to the Identification of Informative Voxel Clusters for Brain State Discrimination , 2008, IEEE Journal of Selected Topics in Signal Processing.

[36]  Stephen C. Strother,et al.  Support vector machines for temporal classification of block design fMRI data , 2005, NeuroImage.

[37]  B. Edin Cutaneous afferents provide information about knee joint movements in humans , 2001, The Journal of physiology.

[38]  M. Raichle,et al.  Tactile-vibration-activated foci in insular and parietal-opercular cortex studied with positron emission tomography: mapping the second somatosensory area in humans. , 1993, Somatosensory & motor research.

[39]  A. Asbury,et al.  The acute sensory neuronopathy syndrome: A distinct clinical entity , 1980, Annals of neurology.

[40]  A. Berti,et al.  Modular structure of awareness for sensorimotor disorders: Evidence from anosognosia for hemiplegia and anosognosia for hemianaesthesia , 2008, Neuropsychologia.

[41]  A. Light,et al.  Spinal laminae I-II neurons in rat recorded in vivo in whole cell, tight seal configuration: properties and opioid responses. , 1999, Journal of neurophysiology.

[42]  F. Tong,et al.  Decoding the visual and subjective contents of the human brain , 2005, Nature Neuroscience.

[43]  A. Craig,et al.  A distinct thermoreceptive subregion of lamina I in nucleus caudalis of the owl monkey , 1999, The Journal of comparative neurology.

[44]  A. Craig,et al.  Quantitative response characteristics of thermoreceptive and nociceptive lamina I spinothalamic neurons in the cat. , 2001, Journal of neurophysiology.

[45]  A. Craig,et al.  Retrograde analyses of spinothalamic projections in the macaque monkey: Input to posterolateral thalamus , 2006, The Journal of comparative neurology.

[46]  J. M. Ritchie,et al.  Non‐medullated fibres in the saphenous nerve which signal touch , 1957, The Journal of physiology.

[47]  J. Dostrovsky,et al.  Cooling-specific spinothalamic neurons in the monkey. , 1996, Journal of neurophysiology.

[48]  Johan Wessberg,et al.  A system of unmyelinated afferents for innocuous mechanoreception in the human skin , 1993, Brain Research.

[49]  G. Essick,et al.  Psychophysical assessment of the affective components of non-painful touch. , 1999, Neuroreport.

[50]  Rainer Goebel,et al.  Combining multivariate voxel selection and support vector machines for mapping and classification of fMRI spatial patterns , 2008, NeuroImage.

[51]  W. Willis,et al.  A critical review of the role of the proposed VMpo nucleus in pain. , 2002, The journal of pain : official journal of the American Pain Society.

[52]  Janaina Mourão Miranda,et al.  Classifying brain states and determining the discriminating activation patterns: Support Vector Machine on functional MRI data , 2005, NeuroImage.

[53]  E. Reiman,et al.  Thermosensory activation of insular cortex , 2000, Nature Neuroscience.

[54]  J. Wessberg,et al.  The neurophysiology of unmyelinated tactile afferents , 2010, Neuroscience & Biobehavioral Reviews.