Primary somatosensory cortex discriminates affective significance in social touch

Another person’s caress is one of the most powerful of all emotional social signals. How much the primary somatosensory cortices (SIs) participate in processing the pleasantness of such social touch remains unclear. Although ample empirical evidence supports the role of the insula in affective processing of touch, here we argue that SI might be more involved in affective processing than previously thought by showing that the response in SI to a sensual caress is modified by the perceived sex of the caresser. In a functional MRI study, we manipulated the perceived affective quality of a caress independently of the sensory properties at the skin: heterosexual males believed they were sensually caressed by either a man or woman, although the caress was in fact invariantly delivered by a female blind to condition type. Independent analyses showed that SI encoded, and was modulated by, the visual sex of the caress, and that this effect is unlikely to originate from the insula. This suggests that current models may underestimate the role played by SI in the affective processing of social touch.

[1]  M. Raichle,et al.  Blood flow changes in human somatosensory cortex during anticipated stimulation , 1995, Nature.

[2]  Gaspare Galati,et al.  Empathic neural reactivity to noxious stimuli delivered to body parts and non‐corporeal objects , 2008, The European journal of neuroscience.

[3]  R. Adolphs,et al.  A Role for Somatosensory Cortices in the Visual Recognition of Emotion as Revealed by Three-Dimensional Lesion Mapping , 2000, The Journal of Neuroscience.

[4]  Angela R. Laird,et al.  ALE meta-analysis of action observation and imitation in the human brain , 2010, NeuroImage.

[5]  Robert Chen,et al.  Digit somatotopy within cortical areas of the postcentral gyrus in humans. , 2008, Cerebral cortex.

[6]  L. Fogassi,et al.  Audiovisual mirror neurons and action recognition , 2003, Experimental Brain Research.

[7]  Michael Erb,et al.  Visual features of an observed agent do not modulate human brain activity during action observation , 2009, NeuroImage.

[8]  Hanna Damasio,et al.  Seeing touch is correlated with content-specific activity in primary somatosensory cortex. , 2011, Cerebral cortex.

[9]  Nava Rubin,et al.  Brain areas selective for both observed and executed movements. , 2007, Journal of neurophysiology.

[10]  Edmund T Rolls,et al.  Convergence of sensory systems in the orbitofrontal cortex in primates and brain design for emotion. , 2004, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[11]  J. Dostrovsky,et al.  Pain-related neurons in the human cingulate cortex , 1999, Nature Neuroscience.

[12]  R. M. Carter Explicit and Implicit Processes in Human Aversive Conditioning , 2006 .

[13]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

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

[15]  P. Andersen,et al.  International Patterns of Interpersonal Tactile Communication: A Field Study , 1998 .

[16]  G. Luppino,et al.  Cortical connections of the inferior parietal cortical convexity of the macaque monkey. , 2006, Cerebral cortex.

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

[18]  C. Keysers,et al.  Empathy and the Somatotopic Auditory Mirror System in Humans , 2006, Current Biology.

[19]  Christian Keysers,et al.  Empathy for positive and negative emotions in the gustatory cortex , 2007, NeuroImage.

[20]  Hiroaki Ishida,et al.  Shared Mapping of Own and Others' Bodies in Visuotactile Bimodal Area of Monkey Parietal Cortex , 2010, Journal of Cognitive Neuroscience.

[21]  Nikolaus Kriegeskorte,et al.  Analyzing for information, not activation, to exploit high-resolution fMRI , 2007, NeuroImage.

[22]  H Burton,et al.  Attending to and Remembering Tactile Stimuli: A Review of Brain Imaging Data and Single-Neuron Responses , 2000, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[23]  M. W. Lustig,et al.  Opposite sex touch avoidance: A national replication and extension , 1987 .

[24]  Malin Björnsdotter,et al.  Vicarious Responses to Social Touch in Posterior Insular Cortex Are Tuned to Pleasant Caressing Speeds , 2011, The Journal of Neuroscience.

[25]  C. Spence,et al.  The science of interpersonal touch: An overview , 2010, Neuroscience & Biobehavioral Reviews.

[26]  Claus Lamm,et al.  How Do We Empathize with Someone Who Is Not Like Us? A Functional Magnetic Resonance Imaging Study , 2010, Journal of Cognitive Neuroscience.

[27]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[28]  A. D’Ausilio,et al.  An fMRI investigation on image generation in different sensory modalities: the influence of vividness. , 2009, Acta psychologica.

[29]  R. E Passingham,et al.  Activations related to “mirror” and “canonical” neurones in the human brain: an fMRI study , 2003, NeuroImage.

[30]  Christian Keysers,et al.  Expanding the mirror: vicarious activity for actions, emotions, and sensations , 2009, Current Opinion in Neurobiology.

[31]  Tom M. Mitchell,et al.  Machine learning classifiers and fMRI: A tutorial overview , 2009, NeuroImage.

[32]  Joaquín M. Fuster,et al.  Neuronal activity of somatosensory cortex in a cross-modal (visuo-haptic) memory task , 1997, Experimental Brain Research.

[33]  E T Rolls,et al.  Representations of pleasant and painful touch in the human orbitofrontal and cingulate cortices. , 2003, Cerebral cortex.

[34]  J. Dreher,et al.  The Architecture of Reward Value Coding in the Human Orbitofrontal Cortex , 2010, The Journal of Neuroscience.

[35]  J. Ward,et al.  Mirror-touch synesthesia is linked with empathy , 2007, Nature Neuroscience.

[36]  Robin I. M. Dunbar The social role of touch in humans and primates: Behavioural function and neurobiological mechanisms , 2010, Neuroscience & Biobehavioral Reviews.

[37]  Martin P. Paulus,et al.  Anterior insular cortex anticipates impending stimulus significance , 2009, NeuroImage.

[38]  V. Andrew Stenger,et al.  Cerebral activation during hypnotically induced and imagined pain , 2004, NeuroImage.

[39]  Francis McGlone,et al.  Sensory and affective judgments of skin during inter- and intrapersonal touch. , 2009, Acta psychologica.

[40]  M. Kringelbach The human orbitofrontal cortex: linking reward to hedonic experience , 2005, Nature Reviews Neuroscience.

[41]  M. Behrmann,et al.  Parietal cortex and attention , 2004, Current Opinion in Neurobiology.

[42]  J. Price,et al.  Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys , 1995, The Journal of comparative neurology.

[43]  A. Meltzoff,et al.  Empathy examined through the neural mechanisms involved in imagining how I feel versus how you feel pain , 2006, Neuropsychologia.

[44]  Nadia Bolognini,et al.  Somatic and Motor Components of Action Simulation , 2007, Current Biology.

[45]  Jonathan D. Nelson,et al.  Human cortical representations for reaching: Mirror neurons for execution, observation, and imagery , 2007, NeuroImage.

[46]  Christian Keysers,et al.  The anthropomorphic brain: The mirror neuron system responds to human and robotic actions , 2007, NeuroImage.

[47]  Christian Keysers,et al.  Somatosensation in social perception , 2010, Nature Reviews Neuroscience.

[48]  Salvatore Maria Aglioti,et al.  Empathy for pain and touch in the human somatosensory cortex. , 2007, Cerebral cortex.

[49]  S. Kühn,et al.  A quantitative meta-analysis on cue-induced male sexual arousal. , 2011, The journal of sexual medicine.

[50]  Vittorio Gallese,et al.  Differential Involvement of Somatosensory and Interoceptive Cortices during the Observation of Affective Touch , 2011, Journal of Cognitive Neuroscience.

[51]  A. Thron,et al.  Clinical hypnosis modulates functional magnetic resonance imaging signal intensities and pain perception in a thermal stimulation paradigm. , 2004, Regional anesthesia and pain medicine.

[52]  Andrew N. Meltzoff,et al.  How do we perceive the pain of others? A window into the neural processes involved in empathy , 2005, NeuroImage.

[53]  C. B. Crawford Effects of Sex and Sex Roles on Avoidance of Same- and Opposite-Sex Touch , 1994, Perceptual and motor skills.

[54]  E. Rolls,et al.  The representation of pleasant touch in the brain and its relationship with taste and olfactory areas. , 1999, Neuroreport.

[55]  Jean Decety,et al.  Motivation modulates the activity of the human mirror-neuron system. , 2007, Cerebral cortex.

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

[57]  Claus Lamm,et al.  Is the extrastriate body area (EBA) sensitive to the perception of pain in others? , 2008, Cerebral cortex.

[58]  Francis McGlone,et al.  Cognitive influences on the affective representation of touch and the sight of touch in the human brain. , 2008, Social cognitive and affective neuroscience.

[59]  Randall Stilla,et al.  Selective visuo‐haptic processing of shape and texture , 2008, Human brain mapping.

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

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

[62]  Nikolaus Kriegeskorte,et al.  How does an fMRI voxel sample the neuronal activity pattern: Compact-kernel or complex spatiotemporal filter? , 2010, NeuroImage.

[63]  Yasuhito Sawahata,et al.  Spatial smoothing hurts localization but not information: Pitfalls for brain mappers , 2010, NeuroImage.

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

[65]  John H. R. Maunsell,et al.  The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[66]  J. Kaas,et al.  Corticocortical connections of area 2 of somatosensory cortex in macaque monkeys: A correlative anatomical and electrophysiological study , 1986, The Journal of comparative neurology.

[67]  Edmund T. Rolls,et al.  Warm pleasant feelings in the brain , 2008, NeuroImage.

[68]  Viviana Betti,et al.  Seeing the pain of others while being in pain: A laser-evoked potentials study , 2008, NeuroImage.

[69]  S-J Blakemore,et al.  Somatosensory activations during the observation of touch and a case of vision-touch synaesthesia. , 2005, Brain : a journal of neurology.

[70]  C. Keysers,et al.  The Observation and Execution of Actions Share Motor and Somatosensory Voxels in all Tested Subjects: Single-Subject Analyses of Unsmoothed fMRI Data , 2008, Cerebral cortex.

[71]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

[72]  Christian Keysers,et al.  Testing Simulation Theory with Cross-Modal Multivariate Classification of fMRI Data , 2008, PloS one.

[73]  Paul E. Downing,et al.  Organization of felt and seen pain responses in anterior cingulate cortex , 2007, NeuroImage.

[74]  Danielle Z. Bolling,et al.  Brain mechanisms for processing affective touch , 2013, Human brain mapping.

[75]  M. Bushnell,et al.  Pain affect encoded in human anterior cingulate but not somatosensory cortex. , 1997, Science.

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

[77]  G. Pellegrino,et al.  Vicarious responses to pain in anterior cingulate cortex: Is empathy a multisensory issue? , 2004, Cognitive, affective & behavioral neuroscience.

[78]  Stefan Pollmann,et al.  Neuroinformatics Original Research Article Pymvpa: a Unifying Approach to the Analysis of Neuroscientifi C Data , 2022 .

[79]  Seung-Schik Yoo,et al.  Neural substrates of tactile imagery: a functional MRI study , 2003, Neuroreport.

[80]  Harold Burton,et al.  Cortical network for vibrotactile attention: A fMRI study , 2008, Human brain mapping.

[81]  D. Pitcher,et al.  Transcranial Magnetic Stimulation Disrupts the Perception and Embodiment of Facial Expressions , 2008, The Journal of Neuroscience.

[82]  M. Jeannerod Neural Simulation of Action: A Unifying Mechanism for Motor Cognition , 2001, NeuroImage.

[83]  Claus Lamm,et al.  What Are You Feeling? Using Functional Magnetic Resonance Imaging to Assess the Modulation of Sensory and Affective Responses during Empathy for Pain , 2007, PloS one.

[84]  H. Barbas Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey , 1988, The Journal of comparative neurology.

[85]  H. Olausson,et al.  The skin as a social organ , 2010, Experimental Brain Research.