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Brain Processing of Reward for Touch, Temperature, and Oral Texture

  • Edmund T. RollsEmail author
Chapter

Abstract

Some of the principles of the representation of affective touch in the brain are described. Positively affective touch and temperature are represented in parts of the orbitofrontal and pregenual cingulate cortex in which other neurons represent the reward value of taste, olfactory, and/or visual stimuli. The orbitofrontal cortex is implicated in some of the affective aspects of touch that may be mediated through C fibre Touch afferents, in that it is activated more by light touch to the forearm (a source of CT afferents) than by light touch to the glabrous skin of the hand. Oral somatosensory afferents implicated in sensing the texture of food including fat in the mouth also activate the orbitofrontal and pregenual cingulate cortex, as well as the insular taste cortex. Top-down cognitive modulation of the representation of affective touch produced by word labels is found in parietal cortex area 7, the insula and ventral striatum. The cognitive labels also influence activations to the sight of touch and also the correlations with pleasantness in the pregenual cingulate/orbitofrontal cortex and ventral striatum.

Keywords

Affective touch Temperature Cognitive modulation Attention Biassed competition Taste Fat texture Pleasure Emotion 

Notes

Acknowledgement

The author acknowledges the collaborative research performed with many colleagues, including I. de Araujo, A. Bilderbeck, H. Critchley, F. Grabenhorst, M. Kadohisa, M. Kringelbach, C. McCabe, F. McGlone, J. O’Doherty, and J. Verhagen, and support from the Medical Research Council.

References

  1. Ackerley R, Backlund Wasling H, Liljencrantz J, Olausson H, Johnson RD, Wessberg J (2014) Human C-tactile afferents are tuned to the temperature of a skin-stroking caress. J Neurosci 34(8):2879–2883. doi: 10.1523/JNEUROSCI.2847-13.2014 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Baumgartner U, Iannetti GD, Zambreanu L, Stoeter P, Treede RD, Tracey I (2010) Multiple somatotopic representations of heat and mechanical pain in the operculo-insular cortex: a high-resolution fMRI study. J Neurophysiol 104(5):2863–2872. doi: 10.1152/jn.00253.2010 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bjornsdotter M, Morrison I, Olausson H (2010) Feeling good: on the role of C fiber mediated touch in interoception. Exp Brain Res 207(3-4):149–155. doi: 10.1007/s00221-010-2408-y CrossRefPubMedGoogle Scholar
  4. Blakemore SJ, Bristow D, Bird G, Frith C, Ward J (2005) Somatosensory activations during the observation of touch and a case of vision-touch synaesthesia. Brain 128(Pt 7):1571–1583CrossRefPubMedGoogle Scholar
  5. Brodersen KH, Wiech K, Lomakina EI, Lin CS, Buhmann JM, Bingel U et al (2012) Decoding the perception of pain from fMRI using multivariate pattern analysis. Neuroimage 63(3):1162–1170. doi: 10.1016/j.neuroimage.2012.08.035 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bufalari I, Aprile T, Avenanti A, Di Russo F, Aglioti SM (2007) Empathy for pain and touch in the human somatosensory cortex. Cereb Cortex 17:2553–2561CrossRefPubMedGoogle Scholar
  7. Carlsson K, Petrovic P, Skare S, Petersson KM, Ingvar M (2000) Tickling expectations: neural processing in anticipation of a sensory stimulus. J Cogn Neurosci 12(4):691–703CrossRefPubMedGoogle Scholar
  8. Craig AD (2002) How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 3(8):655–666CrossRefPubMedGoogle Scholar
  9. Critchley HD, Harrison NA (2013) Visceral influences on brain and behavior. Neuron 77(4):624–638. doi: 10.1016/j.neuron.2013.02.008 CrossRefPubMedGoogle Scholar
  10. Critchley HD, Rolls ET (1996) Responses of primate taste cortex neurons to the astringent tastant tannic acid. Chem Senses 21:135–145CrossRefPubMedGoogle Scholar
  11. Critchley HD, Wiens S, Rotshtein P, Ohman A, Dolan RJ (2004) Neural systems supporting interoceptive awareness. Nat Neurosci 7(2):189–195CrossRefPubMedGoogle Scholar
  12. de Araujo IET, Rolls ET (2004) The representation in the human brain of food texture and oral fat. J Neurosci 24:3086–3093CrossRefPubMedGoogle Scholar
  13. de Araujo IET, Kringelbach ML, Rolls ET, Hobden P (2003) The representation of umami taste in the human brain. J Neurophysiol 90:313–319CrossRefPubMedGoogle Scholar
  14. de Araujo IET, Rolls ET, Velazco MI, Margot C, Cayeux I (2005) Cognitive modulation of olfactory processing. Neuron 46:671–679CrossRefPubMedGoogle Scholar
  15. Deco G, Rolls ET (2006) Decision-making and Weber’s Law: a neurophysiological model. Eur J Neurosci 24:901–916CrossRefPubMedGoogle Scholar
  16. Deco G, Rolls ET, Romo R (2009) Stochastic dynamics as a principle of brain function. Prog Neurobiol 88:1–16CrossRefPubMedGoogle Scholar
  17. Deco G, Rolls ET, Albantakis L, Romo R (2013) Brain mechanisms for perceptual and reward-related decision-making. Prog Neurobiol 103:194–213CrossRefPubMedGoogle Scholar
  18. Fiorio M, Haggard P (2005) Viewing the body prepares the brain for touch: effects of TMS over somatosensory cortex. Eur J Neurosci 22(3):773–777CrossRefPubMedGoogle Scholar
  19. Ge T, Feng J, Grabenhorst F, Rolls ET (2012) Componential Granger causality, and its application to identifying the source and mechanisms of the top-down biased activation that controls attention to affective vs sensory processing. Neuroimage 59:1846–1858CrossRefPubMedGoogle Scholar
  20. Grabenhorst F, Rolls ET (2010) Attentional modulation of affective vs sensory processing: functional connectivity and a top-down biased activation theory of selective attention. J Neurophysiol 104:1649–1660CrossRefPubMedGoogle Scholar
  21. Grabenhorst F, Rolls ET (2011) Value, pleasure, and choice in the ventral prefrontal cortex. Trends Cogn Sci 15:56–67CrossRefPubMedGoogle Scholar
  22. Grabenhorst F, Rolls ET, Bilderbeck A (2008a) How cognition modulates affective responses to taste and flavor: top down influences on the orbitofrontal and pregenual cingulate cortices. Cereb Cortex 18:1549–1559CrossRefPubMedGoogle Scholar
  23. Grabenhorst F, Rolls ET, Parris BA (2008b) From affective value to decision-making in the prefrontal cortex. Eur J Neurosci 28:1930–1939CrossRefPubMedGoogle Scholar
  24. Grabenhorst F, Rolls ET, Parris BA, D’Souza A (2010) How the brain represents the reward value of fat in the mouth. Cereb Cortex 20:1082–1091CrossRefPubMedGoogle Scholar
  25. Guest S, Grabenhorst F, Essick G, Chen Y, Young M, McGlone F et al (2007) Human cortical representation of oral temperature. Physiol Behav 92:975–984CrossRefPubMedGoogle Scholar
  26. Iacoboni M, Molnar-Szakacs I, Gallese V, Buccino G, Mazziotta JC, Rizzolatti G (2005) Grasping the intentions of others with one’s own mirror neuron system. PLoS Biol 3(3):e79CrossRefPubMedPubMedCentralGoogle Scholar
  27. Johansen-Berg H, Lloyd DM (2000) The physiology and psychology of selective attention to touch. Front Biosci 5:D894–D904CrossRefPubMedGoogle Scholar
  28. Kadohisa M, Rolls ET, Verhagen JV (2004) Orbitofrontal cortex neuronal representation of temperature and capsaicin in the mouth. Neuroscience 127:207–221CrossRefPubMedGoogle Scholar
  29. Kadohisa M, Rolls ET, Verhagen JV (2005a) Neuronal representations of stimuli in the mouth: the primate insular taste cortex, orbitofrontal cortex, and amygdala. Chem Senses 30:401–419CrossRefPubMedGoogle Scholar
  30. Kadohisa M, Rolls ET, Verhagen JV (2005b) The primate amygdala: neuronal representations of the viscosity, fat texture, temperature, grittiness and taste of foods. Neuroscience 132:33–48CrossRefPubMedGoogle Scholar
  31. Kobayashi S (2012) Organization of neural systems for aversive information processing: pain, error, and punishment. Front Neurosci 6:136. doi: 10.3389/fnins.2012.00136 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Koski L, Wohlschlager A, Bekkering H, Woods RP, Dubeau MC, Mazziotta JC et al (2002) Modulation of motor and premotor activity during imitation of target-directed actions. Cereb Cortex 12(8):847–855CrossRefPubMedGoogle Scholar
  33. Kringelbach ML, O’Doherty J, Rolls ET, Andrews C (2003) Activation of the human orbitofrontal cortex to a liquid food stimulus is correlated with its subjective pleasantness. Cereb Cortex 13:1064–1071CrossRefPubMedGoogle Scholar
  34. McCabe C, Rolls ET, Bilderbeck A, McGlone F (2008) Cognitive influences on the affective representation of touch and the sight of touch in the human brain. Soc Cogn Affect Neurosci 3:97–108CrossRefPubMedPubMedCentralGoogle Scholar
  35. McGlone F, Vallbo AB, Olausson H, Loken L, Wessberg J (2007) Discriminative touch and emotional touch. Can J Exp Psychol 61(3):173–183CrossRefPubMedGoogle Scholar
  36. McGlone F, Olausson H, Boyle JA, Jones-Gotman M, Dancer C, Guest S et al (2012) Touching and feeling: differences in pleasant touch processing between glabrous and hairy skin in humans. Eur J Neurosci 35(11):1782–1788. doi: 10.1111/j.1460-9568.2012.08092.x CrossRefPubMedGoogle Scholar
  37. Montoya P, Sitges C (2006) Affective modulation of somatosensory-evoked potentials elicited by tactile stimulation. Brain Res 1068(1):205–212CrossRefPubMedGoogle Scholar
  38. Morrison I, Bjornsdotter M, Olausson H (2011) Vicarious responses to social touch in posterior insular cortex are tuned to pleasant caressing speeds. J Neurosci 31(26):9554–9562. doi: 10.1523/JNEUROSCI.0397-11.2011 CrossRefPubMedGoogle Scholar
  39. O’Doherty J, Kringelbach ML, Rolls ET, Hornak J, Andrews C (2001) Abstract reward and punishment representations in the human orbitofrontal cortex. Nat Neurosci 4:95–102CrossRefPubMedGoogle Scholar
  40. Olausson H, Lamarre Y, Backlund H, Morin C, Wallin BG, Starck G et al (2002) Unmyelinated tactile afferents signal touch and project to insular cortex. Nat Neurosci 5(9):900–904CrossRefPubMedGoogle Scholar
  41. Olausson H, Cole J, Rylander K, McGlone F, Lamarre Y, Wallin BG et al (2008) Functional role of unmyelinated tactile afferents in human hairy skin: sympathetic response and perceptual localization. Exp Brain Res 184(1):135–140CrossRefPubMedGoogle Scholar
  42. Pritchard TC, Hamilton RB, Morse JR, Norgren R (1986) Projections of thalamic gustatory and lingual areas in the monkey, Macaca fascicularis. J Comp Neurol 244:213–228CrossRefPubMedGoogle Scholar
  43. Pritchard TC, Edwards EM, Smith CA, Hilgert KG, Gavlick AM, Maryniak TD et al (2005) Gustatory neural responses in the medial orbitofrontal cortex of the old world monkey. J Neurosci 25:6047–6056CrossRefPubMedGoogle Scholar
  44. Pritchard TC, Schwartz GJ, Scott TR (2007) Taste in the medial orbitofrontal cortex of the macaque. Ann N Y Acad Sci 1121:121–135. doi: 10.1196/annals.1401.007, annals.1401.007 [pii]CrossRefPubMedGoogle Scholar
  45. Ramirez I (1994) Chemosensory similarities among oils: does viscosity play a role? Chem Senses 19:155–168CrossRefPubMedGoogle Scholar
  46. Rolls ET (1998) Taste and olfactory processing in the brain, and its relation to the control of eating. Front Oral Biol 9:40–75CrossRefGoogle Scholar
  47. Rolls ET (1999) The brain and emotion. Oxford University Press, OxfordGoogle Scholar
  48. Rolls ET (2000) Neurophysiology and functions of the primate amygdala, and the neural basis of emotion. In: Aggleton JP (ed) The amygdala: a functional analysis, 2nd edn. Oxford University Press, Oxford, pp 447–478Google Scholar
  49. Rolls ET (2005) Emotion explained. Oxford University Press, OxfordCrossRefGoogle Scholar
  50. Rolls ET (2006) Brain mechanisms underlying flavour and appetite. Philos Trans R Soc Lond B Biol Sci 361:1123–1136CrossRefPubMedPubMedCentralGoogle Scholar
  51. Rolls ET (2007a) Sensory processing in the brain related to the control of food intake. Proc Nutr Soc 66:96–112CrossRefPubMedGoogle Scholar
  52. Rolls ET (2007b) Understanding the mechanisms of food intake and obesity. Obes Rev 8(Suppl 1): 67–72CrossRefPubMedGoogle Scholar
  53. Rolls ET (2008a) Functions of the orbitofrontal and pregenual cingulate cortex in taste, olfaction, appetite and emotion. Acta Physiol Hung 95:131–164CrossRefPubMedGoogle Scholar
  54. Rolls ET (2008b) Memory, attention, and decision-making: a unifying computational neuroscience approach. Oxford University Press, OxfordGoogle Scholar
  55. Rolls ET (2010) The affective and cognitive processing of touch, oral texture, and temperature in the brain. Neurosci Biobehav Rev 34:237–245CrossRefPubMedGoogle Scholar
  56. Rolls ET (2011) The neural representation of oral texture including fat texture. J Texture Stud 42:137–156CrossRefGoogle Scholar
  57. Rolls ET (2012) Taste, olfactory, and food texture reward processing in the brain and the control of appetite. Proc Nutr Soc 71:488–501CrossRefPubMedGoogle Scholar
  58. Rolls ET (2013) A biased activation theory of the cognitive and attentional modulation of emotion. Front Hum Neurosci 7(74):1–15Google Scholar
  59. Rolls ET (2014) Emotion and decision-making explained. Oxford University Press, OxfordGoogle Scholar
  60. Rolls ET (2015) Taste, olfactory, and food reward value processing in the brain. Prog Neurobiol 127-128:90–64CrossRefGoogle Scholar
  61. Rolls ET, Baylis LL (1994) Gustatory, olfactory, and visual convergence within the primate orbitofrontal cortex. J Neurosci 14:5437–5452PubMedGoogle Scholar
  62. Rolls ET, Deco G (2010) The noisy brain: stochastic dynamics as a principle of brain function. Oxford University Press, OxfordCrossRefGoogle Scholar
  63. Rolls ET, Grabenhorst F (2008) The orbitofrontal cortex and beyond: from affect to decision-making. Prog Neurobiol 86:216–244CrossRefPubMedGoogle Scholar
  64. Rolls ET, Scott TR (2003) Central taste anatomy and neurophysiology. In: Doty RL (ed) Handbook of olfaction and gustation, 2nd edn. Dekker, New York, pp 679–705Google Scholar
  65. Rolls ET, Yaxley S, Sienkiewicz ZJ (1990) Gustatory responses of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey. J Neurophysiol 64:1055–1066PubMedGoogle Scholar
  66. Rolls ET, Critchley H, Wakeman EA, Mason R (1996) Responses of neurons in the primate taste cortex to the glutamate ion and to inosine 5′-monophosphate. Physiol Behav 59:991–1000CrossRefPubMedGoogle Scholar
  67. Rolls ET, Critchley HD, Browning AS, Hernadi A, Lenard L (1999) Responses to the sensory properties of fat of neurons in the primate orbitofrontal cortex. J Neurosci 19:1532–1540PubMedGoogle Scholar
  68. Rolls ET, Kringelbach ML, de Araujo IET (2003a) Different representations of pleasant and unpleasant odors in the human brain. Eur J Neurosci 18:695–703CrossRefPubMedGoogle Scholar
  69. Rolls ET, O’Doherty J, Kringelbach ML, Francis S, Bowtell R, McGlone F (2003b) Representations of pleasant and painful touch in the human orbitofrontal and cingulate cortices. Cereb Cortex 13:308–317CrossRefPubMedGoogle Scholar
  70. Rolls ET, Verhagen JV, Kadohisa M (2003c) Representations of the texture of food in the primate orbitofrontal cortex: neurons responding to viscosity, grittiness and capsaicin. J Neurophysiol 90:3711–3724CrossRefPubMedGoogle Scholar
  71. Rolls ET, Grabenhorst F, Parris BA (2008) Warm pleasant feelings in the brain. Neuroimage 41:1504–1513CrossRefPubMedGoogle Scholar
  72. Rolls ET, Grabenhorst F, Parris BA (2010) Neural systems underlying decisions about affective odors. J Cogn Neurosci 22:1069–1082CrossRefPubMedGoogle Scholar
  73. Schaefer M, Flor H, Heinze HJ, Rotte M (2006) Dynamic modulation of the primary somatosensory cortex during seeing and feeling a touched hand. Neuroimage 29(2):587–592CrossRefPubMedGoogle Scholar
  74. Singer T, Seymour B, O’Doherty J, Kaube H, Dolan RJ, Frith CD (2004) Empathy for pain involves the affective but not sensory components of pain. Science 303(5661):1157–1162CrossRefPubMedGoogle Scholar
  75. Tsakiris M, Hesse MD, Boy C, Haggard P, Fink GR (2007) Neural signatures of body ownership: a sensory network for bodily self-consciousness. Cereb Cortex 17:2235–2244CrossRefPubMedGoogle Scholar
  76. Umilta MA, Kohler E, Gallese V, Fogassi L, Fadiga L, Keysers C et al (2001) I know what you are doing. A neurophysiological study. Neuron 31(1):155–165CrossRefPubMedGoogle Scholar
  77. Verhagen JV, Rolls ET, Kadohisa M (2003) Neurons in the primate orbitofrontal cortex respond to fat texture independently of viscosity. J Neurophysiol 90:1514–1525CrossRefPubMedGoogle Scholar
  78. Verhagen JV, Kadohisa M, Rolls ET (2004) The primate insular/opercular taste cortex: neuronal representations of the viscosity, fat texture, grittiness, temperature and taste of foods. J Neurophysiol 92:1685–1699CrossRefPubMedGoogle Scholar
  79. Wang XJ (2002) Probabilistic decision making by slow reverberation in cortical circuits. Neuron 36:955–968CrossRefPubMedGoogle Scholar
  80. Wiech K, Tracey I (2013) Pain, decisions, and actions: a motivational perspective. Front Neurosci 7:46. doi: 10.3389/fnins.2013.00046 CrossRefPubMedPubMedCentralGoogle Scholar
  81. Yaxley S, Rolls ET, Sienkiewicz ZJ (1990) Gustatory responses of single neurons in the insula of the macaque monkey. J Neurophysiol 63:689–700PubMedGoogle Scholar
  82. Yoo SS, Freeman DK, McCarthy JJ 3rd, Jolesz FA (2003) Neural substrates of tactile imagery: a functional MRI study. Neuroreport 14(4):581–585CrossRefPubMedGoogle Scholar

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© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Department of Computer ScienceUniversity of Warwick, Coventry CV4 7AL, Oxford Centre for Computational NeuroscienceOxfordUK

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