The effect of age on neural processing of pleasant soft touch stimuli

Frontiers in Behavioral Neuroscience

Volumn 8, Issue FEB, 2014, Pages

  May, April C ^a   Stewart, Jennifer L ^a   Tapert, Susan F ^a,b   Paulus, Martin P ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

Author keywords

Adolescence; CT afferents; Development; FMRI; Insular cortex; Interoception; Reward; Touch

Indexed keywords

EID: 84894234490     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00052     Document Type: Article

References (46)

1. Abraira, V. E., and Ginty, D. D. (2013). The sensory neurons of touch. Neuron 79, 618-639. doi: 10.1016/j.neuron.2013.07.051
2. Ackerley, R., Hassan, E., Curran, A., Wessberg, J., Olausson, H., and Mcglone, F. (2012). An fMRI study on cortical responses during active self-touch and passive touch from others. Front. Behav. Neurosci. 6:51. doi: 10.3389/fnbeh.2012.00051
3. American Psychiatric Association. (2013). Diagnostic and Statistical Manual of Mental Disorders, 5th Edn. Arlington, VA: American Psychiatric Publishing.
4. Benthin, A., Slovic, P., and Severson, H. (1993). A psychometric study of adolescent risk perception. J. Adolesc. 16, 153-168. doi: 10.1006/jado.1993.1014
5. Bjork, J. M., Knutson, B., Fong, G. W., Caggiano, D. M., Bennett, S. M., and Hommer, D. W. (2004). Incentive-elicited brain activation in adolescents: similarities and differences from young adults. J. Neurosci. 24, 1793-1802. doi: 10.1523/JNEUROSCI.4862-03.2004
6. Bjork, J. M., Smith, A. R., Chen, G., and Hommer, D. W. (2010). Adolescents, adults and rewards: comparing motivational neurocircuitry recruitment using fMRI. PLoS ONE 5:e11440. doi: 10.1371/journal.pone.0011440
7. Bjork, J. M., Smith, A. R., Danube, C. L., and Hommer, D. W. (2007). Developmental differences in posterior mesofrontal cortex recruitment by risky rewards. J. Neurosci. 27, 4839-4849. doi: 10.1523/JNEUROSCI.5469-06.2007
8. Bjornsdotter, M., Loken, L., Olausson, H., Vallbo, A., and Wessberg, J. (2009). Somatotopic organization of gentle touch processing in the posterior insular cortex. J. Neurosci. 29, 9314-9320. doi: 10.1523/JNEUROSCI.0400-09.2009
9. Bjornsdotter, M., Morrison, I., and Olausson, H. (2010). Feeling good: on the role of C fiber mediated touch in interoception. Exp. Brain Res. 207, 149-155. doi: 10.1007/s00221-010-2408-y
10. Brodoehl, S., Klingner, C., Stieglitz, K., and Witte, O. W. (2013). Age-related changes in the somatosensory processing of tactile stimulation-an fMRI study. Behav. Brain Res. 238, 259-264. doi: 10.1016/j.bbr.2012.10.038
11. Bush, G., Vogt, B. A., Holmes, J., Dale, A. M., Greve, D., Jenike, M. A., et al. (2002). Dorsal anterior cingulate cortex: a role in reward-based decision making. Proc. Natl. Acad. Sci. U.S.A. 99, 523-528. doi: 10.1073/pnas.012470999
12. Chein, J., Albert, D., O'brien, L., Uckert, K., and Steinberg, L. (2011). Peers increase adolescent risk taking by enhancing activity in the brain's reward circuitry. Dev. Sci. 14, F1-F10. doi: 10.1111/j.1467-7687.2010.01035.x
13. Cohen, J. R., Asarnow, R. F., Sabb, F. W., Bilder, R. M., Bookheimer, S. Y., Knowlton, B. J., et al. (2010). A unique adolescent response to reward prediction errors. Nat. Neurosci. 13, 669-671. doi: 10.1038/nn.2558
14. Cox, R. W. (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 29, 162-173.
15. Craig, A. D. (2002). How do you feel? Interoception: the sense of the physiological condition of the body. Nat. Rev. Neurosci. 3, 655-666. doi: 10.1038/nrn894
16. Craig, A. D. (2003). Interoception: the sense of the physiological condition of the body. Curr. Opin. Neurobiol. 13, 500-505. doi: 10.1016/S0959-4388(03)00090-4
17. Doremus-Fitzwater, T. L., Varlinskaya, E. I., and Spear, L. P. (2010). Motivational systems in adolescence: possible implications for age differences in substance abuse and other risk-taking behaviors. Brain Cogn. 72, 114-123. doi: 10.1016/j.bandc.2009.08.008
18. Eshel, N., Nelson, E. E., Blair, R. J., Pine, D. S., and Ernst, M. (2007). Neural substrates of choice selection in adults and adolescents: development of the ventrolateral prefrontal and anterior cingulate cortices. Neuropsychologia 45, 1270-1279. doi: 10.1016/j.neuropsychologia.2006.10.004
19. Gordon, I., Voos, A. C., Bennett, R. H., Bolling, D. Z., Pelphrey, K. A., and Kaiser, M. D. (2013). Brain mechanisms for processing affective touch. Hum. Brain Mapp. 34, 914-922. doi: 10.1002/hbm.21480
20. Hoffman, E. C., and Mattis, S. G. (2000). A developmental adaptation of panic control treatment for panic disorder in adolescence. Cogn. Behav. Pracitce 7, 253-261. doi: 10.1016/S1077-7229(00)80081-4
21. Keel, P. K., Klump, K. L., Leon, G. R., and Fulkerson, J. A. (1998). Disordered eating in adolescent males from a school-based sample. Int. J. Eat Disord. 23, 125-132.
22. Kessler, R. C., Amminger, G. P., Aguilar-Gaxiola, S., Alonso, J., Lee, S., and Ustun, T. B. (2007). Age of onset of mental disorders: a review of recent literature. Curr. Opin. Psychiatry 20, 359-364. doi: 10.1097/YCO.0b013e32816ebc8c
23. Khalsa, S. S., Rudrauf, D., and Tranel, D. (2009). Interoceptive awareness declines with age. Psychophysiology 46, 1130-1136. doi: 10.1111/j.1469-8986.2009.00859.x
24. Koob, G. F., and Le Moal, M. (2001). Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 24, 97-129. doi: 10.1016/S0893-133X(00)00195-0
25. Kramer, H. H., Lundblad, L., Birklein, F., Linde, M., Karlsson, T., Elam, M., et al. (2007). Activation of the cortical pain network by soft tactile stimulation after injection of sumatriptan. Pain 133, 72-78. doi: 10.1016/j.pain.2007.03.001
26. Lancaster, J. L., Woldorff, M. G., Parsons, L. M., Liotti, M., Freitas, C. S., Rainey, L., et al. (2000). Automated Talairach atlas labels for functional brain mapping. Hum. Brain Mapp. 10, 120-131. doi: 10.1002/1097-0193(200007)10:3<120::AID-HBM30>3.0.CO;2-8
27. Loken, L. S., Wessberg, J., Morrison, I., Mcglone, F., and Olausson, H. (2009). Coding of pleasant touch by unmyelinated afferents in humans. Nat. Neurosci. 12, 547-548. doi: 10.1038/nn.2312
28. McCabe, C., Rolls, E. T., Bilderbeck, A., and 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. doi: 10.1093/scan/nsn005
29. McGlone, F., Olausson, H., Boyle, J. A., 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, 1782-1788. doi: 10.1111/j.1460-9568.2012.08092.x
30. Morrison, I., Bjornsdotter, M., and Olausson, H. (2011a). Vicarious responses to social touch in posterior insular cortex are tuned to pleasant caressing speeds. J. Neurosci. 31, 9554-9562. doi: 10.1523/JNEUROSCI.0397-11.2011
31. Morrison, I., Loken, L. S., Minde, J., Wessberg, J., Perini, I., Nennesmo, I., et al. (2011b). Reduced C-afferent fibre density affects perceived pleasantness and empathy for touch. Brain 134, 1116-1126. doi: 10.1093/brain/awr011
32. Naqvi, N. H., and Bechara, A. (2009). The hidden island of addiction: the insula. Trends Neurosci. 32, 56-67. doi: 10.1016/j.tins.2008.09.009
33. Olausson, H., Lamarre, Y., Backlund, H., Morin, C., Wallin, B. G., Starck, G., et al. (2002). Unmyelinated tactile afferents signal touch and project to insular cortex. Nat. Neurosci. 5, 900-904. doi: 10.1038/nn896
34. Olausson, H., Wessberg, J., and Kakuda, N. (2000). Tactile directional sensibility: peripheral neural mechanisms in man. Brain Res. 866, 178-187. doi: 10.1016/S0006-8993(00)02278-2
35. Olausson, H., Wessberg, J., Morrison, I., Mcglone, F., and Vallbo, A. (2010). The neurophysiology of unmyelinated tactile afferents. Neurosci. Biobehav. Rev. 34, 185-191. doi: 10.1016/j.neubiorev.2008.09.011
36. Patton, J. H., Stanford, M. S., and Barratt, E. S. (1995). Factor structure of the Barratt impulsiveness scale. J. Clin. Psychol. 51, 768-774.
37. Paulus, M. P. (2011). "Interoception and decision making, " in Decision Making, Affect, and Learning, eds M. R. Delgado, E. Phelps, and T. W. Robbins (New York, NY: Oxford University Press), 387-401. doi: 10.1093/acprof:oso/9780199600434.003.0018
38. Paulus, M. P., and Stein, M. B. (2006). An insular view of anxiety. Biol. Psychiatry60, 383-387. doi: 10.1016/j.biopsych.2006.03.042
39. Paulus, M. P., and Stein, M. B. (2010). Interoception in anxiety and depression. Brain Struct. Funct. 214, 451-463. doi: 10.1007/s00429-010-0258-9
40. Paulus, M. P., Tapert, S. F., and Schulteis, G. (2009). The role of interoception and alliesthesia in addiction. Pharmacol. Biochem. Behav. 94, 1-7. doi: 10.1016/j.pbb.2009.08.005
41. Paus, T., Keshavan, M., and Giedd, J. N. (2008). Why do many psychiatric disorders emerge during adolescence? Nat. Rev. Neurosci. 9, 947-957. doi: 10.1038/nrn2513
42. Vallbo, A., Olausson, H., Wessberg, J., and Norrsell, U. (1993). A system of unmyelinated afferents for innocuous mechanoreception in the human skin. Brain Res 628, 301-304.
43. Van Leijenhorst, L., Gunther Moor, B., Op De Macks, Z. A., Rombouts, S. A., Westenberg, P. M., and Crone, E. A. (2010). Adolescent risky decision-making: neurocognitive development of reward and control regions. Neuroimage 51, 345-355. doi: 10.1016/j.neuroimage.2010.02.038
44. Voos, A. C., Pelphrey, K. A., and Kaiser, M. D. (2013). Autistic traits are associated with diminshed neural response to affective touch. Soc. Cogn. Affect. Neurosci. 8, 378-386. doi: 10.1093/scan/nss009
45. Xue, G., Lu, Z., Levin, I. P., and Bechara, A. (2010). The impact of prior risk experiences on subsequent risky decision-making: the role of the insula. Neuroimage 50, 709-716. doi: 10.1016/j.neuroimage.2009.12.097
46. Zuckerman, M. (1996). Item revisions in the sensation seeking scale form V (SSS-V). Pers. Individ. Diff. 20:515.