Representations of pleasant and painful touch in the human orbitofrontal and cingulate cortices.

The cortical areas that represent affectively positive and negative aspects of touch were investigated using functional magnetic resonance imaging (fMRI) by comparing activations produced by pleasant touch, painful touch produced by a stylus, and neutral touch, to the left hand. It was found that regions of the orbitofrontal cortex were activated more by pleasant touch and by painful stimuli than by neutral touch and that different areas of the orbitofrontal cortex were activated by the pleasant and painful touches. The orbitofrontal cortex activation was related to the affective aspects of the touch, in that the somatosensory cortex (SI) was less activated by the pleasant and painful stimuli than by the neutral stimuli. This dissociation was highly significant for both the pleasant touch (P < 0.006) and for the painful stimulus (P < 0.02). Further, it was found that a rostral part of the anterior cingulate cortex was activated by the pleasant stimulus and that a more posterior and dorsal part was activated by the painful stimulus. Regions of the somatosensory cortex, including SI and part of SII in the mid-insula, were activated more by the neutral touch than by the pleasant and painful stimuli. Part of the posterior insula was activated only in the pain condition and different parts of the brainstem, including the central grey, were activated in the pain, pleasant and neutral touch conditions. The results provide evidence that different areas of the human orbitofrontal cortex are involved in representing both pleasant touch and pain, and that dissociable parts of the cingulate cortex are involved in representing pleasant touch and pain.

[1]  Edmund T. Rolls,et al.  Central taste anatomy and neurophysiology. , 2003 .

[2]  E. Rolls The orbitofrontal cortex and reward. , 2000, Cerebral cortex.

[3]  E. Rolls,et al.  Receiving grooming as a reinforcer for the monkey , 1996, Physiology & Behavior.

[4]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[5]  Robert J. Zatorre,et al.  Olfactory identification deficits in patients with focal cerebral excision , 1988, Neuropsychologia.

[6]  W. Freeman,et al.  Psychosurgery in the treatment of mental disorders and intractable pain , 1950 .

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

[8]  B. Vogt,et al.  Nociceptive neurons in area 24 of rabbit cingulate cortex. , 1992, Journal of neurophysiology.

[9]  Edmund T. Rolls,et al.  Neurophysiology and functions of the primate amygdala. , 1992 .

[10]  J D Greenspan,et al.  Stimulus features relevant to the perception of sharpness and mechanically evoked cutaneous pain. , 1991, Somatosensory & motor research.

[11]  E. Rolls,et al.  Hunger and satiety modify the responses of olfactory and visual neurons in the primate orbitofrontal cortex. , 1996, Journal of neurophysiology.

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

[13]  E T Rolls,et al.  Sparseness of the neuronal representation of stimuli in the primate temporal visual cortex. , 1995, Journal of neurophysiology.

[14]  E. Rolls,et al.  Representation of pleasant and aversive taste in the human brain. , 2001, Journal of neurophysiology.

[15]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[16]  D L Rosene,et al.  Thalamic and cortical afferents differentiate anterior from posterior cingulate cortex in the monkey. , 1979, Science.

[17]  E. Rolls,et al.  Abstract reward and punishment representations in the human orbitofrontal cortex , 2001, Nature Neuroscience.

[18]  K. Carlsson,et al.  Tickling Expectations: Neural Processing in Anticipation of a Sensory Stimulus , 2000, Journal of Cognitive Neuroscience.

[19]  F. Mauguière,et al.  Parietal and cingulate processes in central pain. A combined positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) study of an unusual case , 2000, Pain.

[20]  E T Rolls,et al.  Responses to the Sensory Properties of Fat of Neurons in the Primate Orbitofrontal Cortex , 1999, The Journal of Neuroscience.

[21]  T. R. Scott,et al.  Gustatory neural coding in the amygdala of the alert macaque monkey. , 1993, Journal of neurophysiology.

[22]  E. Rolls,et al.  Hunger Modulates the Responses to Gustatory Stimuli of Single Neurons in the Caudolateral Orbitofrontal Cortex of the Macaque Monkey , 1989, The European journal of neuroscience.

[23]  Morten L. Kringelbach,et al.  Fast, Fully Automated Global and Local Magnetic Field Optimization for fMRI of the Human Brain , 2002, NeuroImage.

[24]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

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

[26]  E. Rolls,et al.  Visual responses of neurons in the dorsolateral amygdala of the alert monkey , 1979, Experimental Neurology.

[27]  S. Stone-Elander,et al.  Pain-related cerebral activation is altered by a distracting cognitive task , 2000, Pain.

[28]  R J Zatorre,et al.  Human cortical gustatory areas: a review of functional neuroimaging data. , 1999, Neuroreport.

[29]  N. Costes,et al.  Brain processing of visual sexual stimuli in human males , 2000, Human brain mapping.

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

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

[32]  A. Damasio,et al.  Subcortical and cortical brain activity during the feeling of self-generated emotions , 2000, Nature Neuroscience.

[33]  E. Rolls,et al.  Sensory-specific and motivation-specific satiety for the sight and taste of food and water in man , 1983, Physiology & Behavior.

[34]  E. Rolls,et al.  Gustatory responses of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey. , 1990, Journal of neurophysiology.

[35]  T. Ono,et al.  Gustatory and multimodal neuronal responses in the amygdala during licking and discrimination of sensory stimuli in awake rats. , 1998, Journal of neurophysiology.

[36]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

[37]  H. Critchley,et al.  Neural Activity Relating to Generation and Representation of Galvanic Skin Conductance Responses: A Functional Magnetic Resonance Imaging Study , 2000, The Journal of Neuroscience.

[38]  B. Vogt,et al.  Pain Processing in Four Regions of Human Cingulate Cortex Localized with Co‐registered PET and MR Imaging , 1996, The European journal of neuroscience.

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

[40]  E. Rolls,et al.  Gustatory, olfactory, and visual convergence within the primate orbitofrontal cortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  M. Posner The Brain and Emotion , 1999, Nature Medicine.

[42]  E. Rolls A Theory of Emotion, and its Application to Understanding the Neural Basis of Emotion , 1990 .

[43]  J. Decety,et al.  Neuroanatomical Correlates of Visually Evoked Sexual Arousal in Human Males , 1999, Archives of sexual behavior.

[44]  M. Mesulam,et al.  Insula of the old world monkey. II: Afferent cortical input and comments on the claustrum , 1982, The Journal of comparative neurology.

[45]  T. Paus Primate anterior cingulate cortex: Where motor control, drive and cognition interface , 2001, Nature Reviews Neuroscience.

[46]  C. Geula,et al.  Cytoarchitecture and neural afferents of orbitofrontal cortex in the brain of the monkey , 1992, The Journal of comparative neurology.

[47]  T. Paus,et al.  Functional connectivity of the anterior cingulate cortex within the human frontal lobe: a brain-mapping meta-analysis , 2000, Experimental Brain Research.

[48]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[49]  Jen-Chuen Hsieh,et al.  Central representation of chronic ongoing neuropathic pain studied by positron emission tomography , 1995, PAIN®.

[50]  Karl J. Friston,et al.  A direct quantitative relationship between the functional properties of human and macaque V5 , 2000, Nature Neuroscience.

[51]  D. Wolpert,et al.  Central cancellation of self-produced tickle sensation , 1998, Nature Neuroscience.

[52]  Brian Knutson,et al.  Anticipation of Increasing Monetary Reward Selectively Recruits Nucleus Accumbens , 2001, The Journal of Neuroscience.

[53]  B. Vogt,et al.  Contributions of anterior cingulate cortex to behaviour. , 1995, Brain : a journal of neurology.

[54]  R. J. Dolan,et al.  Differential neural response to positive and negative feedback in planning and guessing tasks , 1997, Neuropsychologia.

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

[56]  Samuel M. McClure,et al.  Predictability Modulates Human Brain Response to Reward , 2001, The Journal of Neuroscience.

[57]  K. Davis,et al.  The neural circuitry of pain as explored with functional MRI , 2000, Neurological research.

[58]  Gregor Thut,et al.  Activation of the human brain by monetary reward , 1997, Neuroreport.

[59]  E. Rolls,et al.  Orbitofrontal cortex neurons: role in olfactory and visual association learning. , 1996, Journal of neurophysiology.

[60]  B. Vogt,et al.  Connections of the Monkey Cingulate Cortex , 1993 .

[61]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[62]  S. Rauch,et al.  Anterior cingulate cortex dysfunction in attention-deficit/hyperactivity disorder revealed by fMRI and the counting stroop , 1999, Biological Psychiatry.

[63]  Martin Ingvar,et al.  Imaging cognitive modulation of pain processing , 2002, Pain.

[64]  D. Collins,et al.  Automatic 3D Intersubject Registration of MR Volumetric Data in Standardized Talairach Space , 1994, Journal of computer assisted tomography.

[65]  T. Paus,et al.  Cerebral Mechanisms of Hypnotic Induction and Suggestion , 1999, Journal of Cognitive Neuroscience.

[66]  R. Buckner,et al.  Human Brain Mapping 6:373–377(1998) � Event-Related fMRI and the Hemodynamic Response , 2022 .

[67]  Wolfgang Grodd,et al.  Functional MRI reveals left amygdala activation during emotion , 1997, Psychiatry Research: Neuroimaging.

[68]  Krish D. Singh,et al.  fMRI of Thermal Pain: Effects of Stimulus Laterality and Attention , 2002, NeuroImage.

[69]  S. Paradiso,et al.  Book Review: Affective Neuroscience: The Foundations of Human and Animal Emotions , 2000 .

[70]  J. Kaas The functional organization of somatosensory cortex in primates. , 1993, Annals of anatomy = Anatomischer Anzeiger : official organ of the Anatomische Gesellschaft.

[71]  E. Rolls,et al.  Olfactory Sensory-Specific Satiety in Humans , 1997, Physiology & Behavior.

[72]  M. Ingvar Pain and functional imaging. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[74]  S. Petersen,et al.  Characterizing the Hemodynamic Response: Effects of Presentation Rate, Sampling Procedure, and the Possibility of Ordering Brain Activity Based on Relative Timing , 2000, NeuroImage.

[75]  Alan C. Evans,et al.  Functional localization and lateralization of human olfactory cortex , 1992, Nature.

[76]  Robin I. M. Dunbar Grooming, Gossip and the Evolution of Language , 1996 .

[77]  K. Berman,et al.  Neural activation during acute capsaicin-evoked pain and allodynia assessed with PET. , 1998, Brain : a journal of neurology.

[78]  E T Rolls,et al.  Sensory‐specific satiety‐related olfactory activation of the human orbitofrontal cortex , 2000, Neuroreport.

[79]  J. Pardo,et al.  Emotion, olfaction, and the human amygdala: amygdala activation during aversive olfactory stimulation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[80]  Frank Munz,et al.  Central activation by histamine-induced itch: analogies to pain processing: a correlational analysis of O-15 H2O positron emission tomography studies , 2001, Pain.

[81]  D. Perrett,et al.  A specific neural substrate for perceiving facial expressions of disgust , 1997, Nature.

[82]  E T Rolls,et al.  Central nervous mechanisms related to feeding and appetite. , 1981, British medical bulletin.

[83]  R. Dolan,et al.  Conscious and unconscious emotional learning in the human amygdala , 1998, Nature.

[84]  J. Mazziotta,et al.  Rapid Automated Algorithm for Aligning and Reslicing PET Images , 1992, Journal of computer assisted tomography.

[85]  S. Rauch,et al.  Response and Habituation of the Human Amygdala during Visual Processing of Facial Expression , 1996, Neuron.

[86]  J. R. Baker,et al.  Imaging subcortical auditory activity in humans , 1998, Human brain mapping.

[87]  David P. Friedman,et al.  Cortical connections of the somatosensory fields of the lateral sulcus of macaques: Evidence for a corticolimbic pathway for touch , 1986, The Journal of comparative neurology.

[88]  Anthony K. P. Jones,et al.  Pain processing during three levels of noxious stimulation produces differential patterns of central activity , 1997, Pain.

[89]  Alan C. Evans,et al.  Emotional responses to pleasant and unpleasant music correlate with activity in paralimbic brain regions , 1999, Nature Neuroscience.