Abstract
Investigating the role of C-tactile (CT) afferents in affective touch requires exploration of the subcortical and cortical brain regions which receive information from the CT afferent pathway. This chapter summarizes the major known cortical targets and wider networks associated with CT-mediated touch, particularly the posterior insula and parietal operculum. It concludes with an outline of three hypotheses regarding the possible function of CT afferents. A central feature of each is the idea that C mechanoreceptive afferents contribute to physiological regulation, particularly of the sympathetic nervous system, in a manner which can extend to the social domain.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abraira VE, Ginty DD (2013) The sensory neurons of touch. Neuron 79:618–639
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 34:2879–2883
Andrew D (2010) Quantitative characterization of low-threshold mechanoreceptor inputs to lamina I spinoparabrachial neurons in the rat. J Physiol 588:117–124
Baumgärtner 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 104:2863–2872
Beauchamp, MS, Yasar NE, Frye RE, Ro, T. (2008) Touch, sound and vision in human superior temporal sulcus. NeuroImage 41:1011–20
Bennett RH, Bolling DZ, Anderson LC, Pelphrey KA, Kaiser MD (2014) fNIRS detects temporal lobe response to affective touch. Soc Cogn Affect Neurosci 9:470–476
Berger CC, Ehrsson HH (2014) The fusion of mental imagery and sensation in the temporal association cortex. J Neurosci 34:13684–13692
Berridge KC, Robinson TE (2003) Parsing reward. Trends Neurosci 26:507–513
Björnsdotter M, Löken L, Olausson H, Vallbo A, Wessberg J (2009) Somatotopic organization of gentle touch processing in the posterior insular cortex. J Neurosci 29:9314–9320
Björnsdotter M, Morrison I, Olausson H (2010) Feeling good: on the role of C fiber mediated touch in interoception. Exp Brain Res 207:149–155
Bolognini N, Rossetti A, Maravita A, Miniussi C (2011) Seeing touch in the somatosensory cortex: a TMS study of the visual perception of touch. Hum Brain Mapp 32:2104–2114
Cauda F, D’Agata F, Sacco K, Duca S, Geminiani G, Vercelli A (2011) Functional connectivity of the insula in the resting brain. Neuroimage 55:8–23
Cerliani L, Thomas RM, Jbabdi S, Siero JC, Nanetti L, Crippa A (2012) Probabilistic tractography recovers a rostrocaudal trajectory of connectivity variability in the human in the insular cortex. Hum Brain Mapp 33:2005–2034
Coan JA, Schaefer HS, Davidson RJ (2006) Lending a hand: social regulation of the neural response to threat. Psychol Sci 17:1032–1039
Craig, AD (1995) Distribution of brainstem projections from spinal lamina I neurons in the cat and the monkey. J Comp Neurol 361:225–48
Craig AD (2002) How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 3:655–666
Craig, AD (2003) Interoception: the sense of the physiological condition of the body Curr Opin Neurobiol 13:500–5
Craig, AD (2004) Human feelings: why are some more aware than others? Trends Cogn Sci 8:239–41
Craig, AD (2009) How do you feel--now? The anterior insula and human awareness. Nature reviews. Neuroscience 10:59–70
Deen B, Pitskel NB, Pelphrey KA (2011) Three systems of insular functional connectivity identified with cluster analysis. Cereb Cortex 7:1498–1506
Disbrow E, Roberts T, Krubitzer L (2000) Somatotopic organization of cortical fields in the lateral sulcus of Homo sapiens: evidence for SII and PV. J Comp Neurol 418:1–21
Dum RP, Levinthal DJ, Strick PL (2009) The spinothalamic system targets motor and sensory areas in the cerebral cortex of monkeys. J Neurosci 29:14223–14235
Ebisch SJ, Ferri F, Salone A, Perrucci MG, D’Amico L, Ferro FM, Romani GL, Gallese V (2011) Differential involvement of somatosensory and interoceptive cortices during the observation of affective touch. J Cogn Neurosci 23:1808–1822
Eickhoff SB, Amunts K, Mohlberg H, Zilles K (2006) Human parietal operculum I. Cytoarchetectonic mapping of subdivisions. Cereb Cortex 16:254–267
Evrard HC, Logothetis NK, Craig AD (2014) Modular architectonic organization of the insula in the macaque monkey. J Comp Neurol 522:64–97
Francis S, ET Rolls ET, Bowtell R, McGlone F, O’Doherty J, Browning A, Clare S, Smith E (1999) The representation of pleasant touch in the brain and its relationship with taste and olfactory areas. Neuroreport 10:453–9
Friedman DP, Murray EA (1986) Thalamic connectivity of the second somatosensory area and neighboring somatosensory fields of the lateral sulcus of the macaque. J Comp Neurol 252:348–373
Friedman DP, Murray EA, O’Neill JB, Mishkin M (1986) Cortical connections of the somatosensory fields of the lateral sulcus of macaques: evidence for a corticolimbic pathway for touch. J Comp Neurol 252:323–347
Gazzola V, Spezio ML, Etzel JA, Castelli F, Adolphs R, Keysers C (2012) Primary somatosensory cortex discriminates affective significance in social touch. Proc Natl Acad Sci U S A 109:E1657–E1666
Ghazanfar AA, Chandrasekaran C, Logothetis NK (2008) Interactions between the superior temporal sulcus and auditory cortex mediate dynamic face/voice integration in rhesus monkeys. J Neurosci 28:4457–4469
Gilbert C, McCafferty DJ, Giroud S, Ancel A, Blanc S (2012) Private heat for public warmth: how huddling shapes individual thermogenic responses of rabbit pups. PLOS One 7(e33553)
Gordon I, Voos AC, Bennett RH, Bolling DZ, Pelphrey KA, Kaiser MD (2011) Brain mechanisms for processing affective touch. Hum Brain Mapp 34:914–922
Gould SJ, Vrba E (1982) Exaptation: a missing term in the science of form. Paleobiology 8:4–15
Gracheva, EO, Bagriantsev, SN (2015) Evolutionary adaptation to thermosensation. Curr Opin Neurobiol 34:67–73
Graziano A, Jones EG (2004) Widespread thalamic terminations of fibers arising in the superficial medullary dorsal horn of monkeys and their relation to calbindin immunoreactivity. J Neurosci 24:248–256
Haim A, Van Aarde RJ, Skinner JD (1992) Burrowing and huddling in newborn porcupine: the effect on thermoregulation. Physiol Behav 52:247–250
Kaiser MD, Yang DY, Voos AC, Bennett RH, Gordon I, Pretzsch C, Beam D, Keifer C, Eilbott J, McGlone F, Pelphrey KA (2015) Brain mechanisms for processing affective (and nonaffective) touch are atypical in autism. Cereb Cortex 26(6):2705–2714, pii: bhv125
Kilintari M, Raos V, Savaki HE (2014) Involvement of the superior temporal cortex in action execution and action observation. J Neurosci 34:8999–9011
Krubitzer LA, Kaas JH (1992) The somatosensory thalamus of monkeys: cortical connections and a redefinition of nuclei in marmosets. J Comp Neurol 319:123–140
Kurth F, Zilles K, Fox PT, Laird AR, Eickhoff SB (2010) A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct Funct 214:519–534
Lindgren L, Westling G, Brulin C, Lehtipalo S, Andersson M, Nyberg L (2012) Pleasant human touch is represented in pregenual anterior cingulate cortex. Neuroimage 59:3427–3432
Löken LS, Wessberg J, Morrison I, McGlone F, Olausson H (2009) Coding of pleasant touch by unmyelinated afferents in humans. Nat Neurosci 5:547–548
Lou S, Pan X, Huang T, Duan B, Yang FC, Yang J, Xiong M, Liu Y, Ma Q (2015) Incoherent feed-forward regulatory loops control segregation of C-mechanoreceptors, nociceptors, and pruriceptors. J Neurosci 35:5317–5329
Lovero KL, Simmons AN, Aron JL, Paulus MP (2009) Anterior insular cortex anticipates impending stimulus significance. Neuroimage 45:976–983
Lucas MV, Anderson LC, Bolling DZ, Pelphrey KA, Kaiser MD (2014) Dissociating the neural correlates of experiencing and imagining affective touch. Cereb Cortex 25(9):2623–2630
Ma Q (2010) Labeled lines meet and talk: population coding of somatic sensations. J Clin Invest 120:3773–3778
Ma Q (2012) Population coding of somatic sensations. Neurosci Bull 28:91–99
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 3:97–108
McGlone F, Olausson H, Boyle JA, Jones-Gotman M, Dancer C, Guest S (2012) Touching and feeling: differences in pleasant touch processing between glabrous and hairy skin in humans. Eur J Neurosci 35:1782–1788
McGlone F, Wessberg J, Olausson H (2014) Discriminative and affective touch: sensing and feeling. Neuron 82:737–755
Migliorini R, Stewart JL, May AC, Tapert SF, Paulus MP (2013) What do you feel? Adolescent drug and alcohol users show altered brain response to pleasant interoceptive stimuli. Drug Alcohol Depend 133:661–668
Morrison, I (in press) Keep calm and cuddle on: social touch as a stress buffer. Adaptive Hum Beh Physiol
Morrison I (2016) ALE meta-analysis reveals distinct networks for affective and discriminatory aspects of touch. Hum Brain Mapp 37:1308–1320
Morrison SF, Nakamura K, Madden CJ (2008) Central control of thermogenesis in mammals. Exp Physiol 93:773–797
Morrison I, Löken LS, Olausson H (2010) The skin as a social organ. Exp Brain Res 204:305–314
Morrison I, Björnsdotter M, Olausson H (2011a) Vicarious responses to social touch in posterior insular cortex are tuned to pleasant caressing speeds. J Neurosci 31:9554–9562
Morrison I, Löken LS, Minde J, Wessberg J, Perini I, Nennesmo I, Olausson H (2011b) Reduced C-afferent fibre density affects perceived pleasantness and empathy for touch. Brain 134:1116–1126
Olausson H, Lamarre Y, Backlund H, Morin C, Wallin BG, Starck G, Ekholm S, Strigo I, Worsley K, Vallbo ÅB, Bushnell MC (2002) Unmyelinated tactile afferents signal touch and project to insular cortex. Nat Neurosci 5:900–904
Olausson H, Wessberg J, Morrison I, McGlone F, Vallbo Å (2010) The neurophysiology of unmyelinated tactile afferents. Neurosci Biobehav Rev 34:185–191
Padoa-Schioppa C, Cai X (2011) The orbitofrontal cortex and the computation of subjective value: consolidated concepts and new perspectives. Ann N Y Acad Sci 1239:130–137
Perini I, Olausson H, Morrison I (2015) Seeking pleasant touch: neural correlates of behavioral preferences for skin stroking. Front Behav Neurosci 9:8. doi:10.3389/fnbeh.2015.00008
Perrett DI, Smith PA, Potter DD, Mistlin AJ, Head AS, Milner AD (1985) Visual cells in the temporal cortex sensitive to face view and gaze direction. Proc R Soc Lond B Biol Sci 223:293–317
Porges SW (2007) The polyvagal perspective. Biol Psychol 74:116–143
Prescott SA, Ma Q, De Koninck Y (2014) Normal and abnormal coding of somatosensory stimuli causing pain. Nat Neurosci 17:183–191
Qi HX, Lyon DC, Kaas JH (2002) Cortical and thalamic connections of the parietal ventral somatosensory area in marmoset monkeys (Callithrix jacchus). J Comp Neurol 443:168–182
Rolls ET, Grabenhorst F (2008) The orbitofrontal cortex and beyond: from affect to decision-making. Prog Neurobiol 86:216–244
Rolls ET, Kringelbach ML, de Araujo IE (2003) Different representations of pleasant and unpleasant odours in the human brain. Eur J Neurosci 18:695–703
Ryu V, Garretson JT, Liu Y, Vaughan CH, Bartness TJ (2015) Brown adipose tissue has sympathetic-sensory feedback circuits. J Neurosci 35:2181–2190
Schirmer A, Jesuthasan S, Mathuru AS (2013) Tactile stimulation reduces fear in fish. Front Behav Neurosci 7:167
Schulkin J (2011) Social allostasis: anticipatory regulation of the internal milieu. Front Evol Neurosci 2:111. doi:10.3389/fnevo.2010.00111
Segerdahl AR, Mezue M, Okell TW, Farrar JT, Tracey I (2015) The dorsal posterior insula subserves a fundamental role in human pain. Nat Neurosci 18:499–500
Seth AK (2013) Interoceptive inference, emotion, and the embodied self. Trends Cogn Sci 17:565–573
Seth AK, Critchley HD (2013) Extending predictive processing to the body: emotion as interoceptive inference. Behav Brain Sci 36:227–228
Sliz D, Smith A, Wiebking C, Northoff G, Hayley S (2012) Neural correlates of a single-session massage treatment. Brain Imaging Behav 6:77–87
Sterling P (2012) Allostasis: a model of predictive regulation. Physiol Behav 106:5–15
Voos AC, Pelphrey KA, Kaiser MD (2013) Autistic traits are associated with diminished neural response to affective touch. Soc Cogn Affect Neurosci 8:378–386
Vrontou S, Wong AM, Rau KK, Koerber HR, Anderson DJ (2013) Genetic identification of C fibres that detect massage-like stroking of hairy skin in vivo. Nature 493:669–673
Wei P, Bao R (2013) The role of insula-associated brain network in touch. Biomed Res Int 2013:734326
Willis WD Jr, Zhang X, Honda CN, Giesler GJ Jr (2002) A critical review of the role of the proposed VMpo nucleus in pain. J Pain 3:79–94
Zimmerman A, Bai L, Ginty DD (2014) The gentle touch receptors of mammalian skin. Science 346:950–954
zu Eulenburg P, Baumgärtner U, Treede RD, Dieterich M (2013) Interoceptive and multimodal functions of the operculo-insular cortex: tactile, nociceptive and vestibular representations. Neuroimage 83:75–86
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer Science+Business Media New York
About this chapter
Cite this chapter
Morrison, I. (2016). CT Afferent-Mediated Affective Touch: Brain Networks and Functional Hypotheses. In: Olausson, H., Wessberg, J., Morrison, I., McGlone, F. (eds) Affective Touch and the Neurophysiology of CT Afferents. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-6418-5_12
Download citation
DOI: https://doi.org/10.1007/978-1-4939-6418-5_12
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4939-6416-1
Online ISBN: 978-1-4939-6418-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)