The man who feels two hearts: The different pathways of interoception

Social Cognitive and Affective Neuroscience

Volumn 9, Issue 9, 2013, Pages 1253-1260

  Couto, Blas ^a,b,c   Salles, Alejo ^b,d   Sedeño, Lucas ^a,b,c   Peradejordi, Margarita ^a   Barttfeld, Pablo ^d,e   Canales Johnson, Andrés ^c,f   Dos Santos, Yamil Vidal ^d   Huepe, David ^c   Bekinschtein, Tristán ^f   Sigman, Mariano ^b,d,g   Favaloro, Roberto ^a   Manes, Facundo ^a   Ibanez, Agustin ^a,b,c  

^a FAVALORO UNIVERSITY   (Argentina)

^b Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^c UNIVERSIDAD DIEGO PORTALES   (Chile)

^d UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^e INSERM   (France)

^f MRC COGNITION AND BRAIN SCIENCES UNIT   (United Kingdom)

^g UNIVERSIDAD TORCUATO DI TELLA   (Argentina)

Author keywords

Heart brain; HEP; Insula; Interoception; Social cognition

Indexed keywords

ADULT; BRAIN CORTEX; COGNITION DISORDERS; COMPLICATION; ELECTROCARDIOGRAPHY; ELECTROENCEPHALOGRAPHY; EMOTION; FEMALE; HEART ASSIST DEVICE; HEART FAILURE; HEART RATE; HUMAN; INTEROCEPTION; MALE; NEUROPSYCHOLOGICAL TEST; PHYSIOLOGY; PSYCHOLOGY; SENSORY NERVE; YOUNG ADULT;

ADULT; AFFERENT PATHWAYS; CEREBRAL CORTEX; COGNITION DISORDERS; ELECTROCARDIOGRAPHY; ELECTROENCEPHALOGRAPHY; EMOTIONS; FEMALE; HEART FAILURE; HEART RATE; HEART-ASSIST DEVICES; HUMANS; INTEROCEPTION; MALE; NEUROPSYCHOLOGICAL TESTS; YOUNG ADULT;

EID: 84908689465     PISSN: 17495016     EISSN: 17495024     Source Type: Journal    
DOI: 10.1093/scan/nst108     Document Type: Article

References (59)

1. Baez, S., Rattazzi, A., Gonzalez-Gadea, M.L., et al. (2012). Integrating intention and context: assessing social cognition in adults with Asperger syndrome. Frontiers in Human Neuroscience, 6, 302.
2. Baron-Cohen, S., Jolliffe, T., Mortimore, C., Robertson, M. (1997). Another advanced test of theory of mind: evidence from very high functioning adults with autism or asperger syndrome. Journal of Child Psychology and Psychiatry, 38(7), 813-22.
3. Bechara, A., Naqvi, N. (2004). Listening to your heart: interoceptive awareness as a gateway to feeling. Nature Neuroscience, 7(2), 102-3.
4. Brainard, D.H. (1997). The psychophysics toolbox. Spatial Vision, 10(4), 433-6.
5. Cameron, O.G. (2002). Visceral Sensory Neuroscience: Interoception. New York: Oxford University Press.
6. Cameron, O.G., Minoshima, S. (2002). Regional brain activation due to pharmacologically induced adrenergic interoceptive stimulation in humans. Psychosomatic Medicine, 64(6), 851-61.
7. Clark, A., Chalmers, D. (1998). The extended mind. Analysis, 58(1), 7-19.
8. Cohen, L.G., Celnik, P., Pascual-Leone, A., et al. (1997). Functional relevance of crossmodal plasticity in blind humans. Nature, 389(6647), 180-3.
9. Couto, B., et al. (2013a). Insular networks for emotional processing and social cognition: Comparison of two case reports with either cortical or subcortical involvement. Cortex, 49, 1420-34.
10. Couto, B., Manes, F., Montañes, P., et al. (2013b). Structural neuroimaging of social cognition in in progressive non-fluent aphasia and behavioral variant of frontotemporal dementia. Front. Hum. Neurosci., 7, 467doi: 10.3389/fnhum.2013.00467.
11. Cox, C.L., et al. (2011). The balance between feeling and knowing: affective and cognitive empathy are reflected in the brain's intrinsic functional dynamics. Social Cognitive and Affective Neuroscience.
12. Craig, A.D. (2002). How do you feel? Interoception: the sense of the physiological condition of the body. Nature Reviews Neuroscience, 3(8), 655-66.
13. Craig, A.D. (2003). Interoception: the sense of the physiological condition of the body. Current Opinion Neurobioliogy, 13(4), 500-5.
14. Critchley, H.D., Wiens, S., Rotshtein, P., et al. (2004). Neural systems supporting interoceptive awareness. Nature Neuroscience, 7(2), 189-95.
15. Domschke, K., Stevens, S., Pfleiderer, B., Gerlach, A.L. (2010). Interoceptive sensitivity in anxiety and anxiety disorders: an overview and integration of neurobiological findings. Clinical Psychology Review, 30(1), 1-11.
16. Dunn, B.D., Galton, H.C., Morgan, R., et al. (2010a). Can you feel the beat? Interoceptive awareness is an interactive function of anxiety-and depression-specific symptom dimensions. Behaviour Research and Therapy, 48(11), 1133-8.
17. Dunn, B.D., Stefanovitch, I., Evans, D., et al. (2010b). Listening to your heart. How interoception shapes emotion experience and intuitive decision making. Psychological Science, 21(12), 1835-44.
18. Dunn, B.D., Evans, D., Makarova, D., White, J., Clark, L. (2012). Gut feelings and the reaction to perceived inequity: the interplay between bodily responses, regulation, and perception shapes the rejection of unfair offers on the ultimatum game. Cognitive and Affective Behavioral Neuroscience, 12(3), 419-29.
19. Fukushima, H., Terasawa, Y., Umeda, S. (2011). Association between interoception and empathy: evidence from heartbeat-evoked brain potential. International Journal of Psychophysiology, 79(2), 259-65.
20. Gray, M.A., Taggart, P., Sutton, P.M., et al. (2007). A cortical potential reflecting cardiac function. Proceedings of the National Academy of Sciences, USA, 104(16), 6818-23.
21. Ibanez, A., Manes, F. (2012). Contextual social cognition and the behavioral variant of frontotemporal dementia. Neurology, 78, 1354-62.
22. Iriki, A., Tanaka, M., Iwamura, Y. (1996). Coding of modified body schema during tool use by macaque postcentral neurones. Neuroreport, 7(14), 2325-30.
23. Katkin, E.S., Wiens, S., Ohman, A. (1982). Individual differences in heartbeat discrimination. Psychophysiology, 19(2), 160-6.
24. Khalsa, S.S., Rudrauf, D., Feinstein, J.S., Tranel, D. (2009a). The pathways of interoceptive awareness. Nature Neuroscience, 12(12), 1494-6.
25. Khalsa, S.S., Rudrauf, D., Sandesara, C., Olshansky, B., Tranel, D. (2009b). Bolus isoproterenol infusions provide a reliable method for assessing interoceptive awareness. International Journal of Psychophysiology, 72(1), 34-45.
26. Kirk, U., Downar, J., Montague, P.R. (2011). Interoception drives increased rational decision-making in meditators playing the ultimatum game. Frontal Neuroscience, 5, 49.
27. Knapp-Kline, K., Kline, J.P. (2005). Heart rate, heart rate variability, and heartbeat detection with the method of constant stimuli: slow and steady wins the race. Biological Psychology, 69(3), 387-96.
28. Lamm, C., Singer, T. (2010). The role of anterior insular cortex in social emotions. Brain Structure and Function, 214(5-6), 579-91.
29. Longhurst, J. (2004). Cardiac and other visceral afferents. In: Roberston, D., editor. Primer on the Autonomic Nervous System. San Diego: Elsevier Academic Press.
30. Lutz, A., Greischar, L.L., Perlman, D.M., Davidson, R.J. (2009). BOLD signal in insula is differentially related to cardiac function during compassion meditation in experts vs. novices. Neuroimage, 47(3), 1038-46.
31. Malafouris, L. (2008). Beads for a plastic mind: the 'blind man's stick' (BMS) hypotheis and the active nature of material culture. Cambridge Archaeological Journal, 18, 401-14.
32. Malafouris, L. (2010). The brain-artefact interface (BAI): a challenge for archaeology and cultural neuroscience. Social Cognitive and Affective Neuroscience, 5(2-3), 264-73.
33. Malafouris, L., Renfrew, C. (2010). Knapping intentions and the marks of the mental. In: The Cognitive Life of Things: Recasting the Boundaries of the Mind. Cambridge: McDonald Institute, pp. 13-22.
34. Malliani, A., Lombardi, F., Pagani, M. (1986). Sensory innervation of the heart. Prog Brain Res, 67, 39-48.
35. Manger, P.R., Woods, T.M., Jones, E.G. (1996). Plasticity of the somatosensory cortical map in macaque monkeys after chronic partial amputation of a digit. Proceedings of the Royal Society B: Biological Sciences, 263(1372), 933-9.
36. Manly, B.F.J. (1997). Randomization, Bootstrap and Monte Carlo Methods in Biology. Boca Raton, FL: Chapman & Hall/CRC.
37. Melloni, M., Lopez, V., Ibanez, A. (2013). Empathy and contextual social cognition. Cogn Affect Behav Neurosci. doi: 10.3758/s13415-013-0205-3.
38. Merzenich, M.M., Kaas, J.H., Wall, J., Nelson, R.J., Sur, M., Felleman, D. (1983). Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation. Neuroscience, 8(1), 33-55.
39. Mikus, E., Stepanenko, A., Krabatsch, T., et al. (2011). Reversibility of fixed pulmonary hypertension in left ventricular assist device support recipients. European Journal Cardiothoracic Surgery, 40(4), 971-7.
40. Mogilner, A., Grossman, J.A., Ribary, U., et al. (1993). Somatosensory cortical plasticity in adult humans revealed by magnetoencephalography. Proceedings of the National Academy of Sciences, USA, 90(8), 3593-7.
41. Ochsner, K.N., Zaki, J., Hanelin, J., et al. (2008). Your pain or mine? Common and distinct neural systems supporting the perception of pain in self and other. Social Cognitive and Affective Neuroscience, 3(2), 144-60.
42. Pollatos, O., Kirsch, W., Schandry, R. (2005). Brain structures involved in interoceptive awareness and cardioafferent signal processing: a dipole source localization study. Human Brain Mapping, 26(1), 54-64.
43. Pollatos, O., Gramann, K., Schandry, R. (2007a). Neural systems connecting interoceptive awareness and feelings. Human Brain Mapping, 28(1), 9-18.
44. Pollatos, O., Schandry, R., Auer, D.P., Kaufmann, C. (2007b). Brain structures mediating cardiovascular arousal and interoceptive awareness. Brain Research, 1141, 178-87.
45. Ramachandran, V.S. (1993). Behavioral and magnetoencephalographic correlates of plasticity in the adult human brain. Proceedings of the National Academy of Sciences USA, 90(22), 10413-20.
46. Rouse, C.H., Jones, G.E., Jones, K.R. (1988). The effect of body composition and gender on cardiac awareness. Psychophysiology, 25, 400-7.
47. Schandry, R. (1981). Heart beat perception and emotional experience. Psychophysiology, 18(4), 483-8.
48. Schandry, R., Weitkunat, R. (1990). Enhancement of heartbeat-related brain potentials through cardiac awareness training. International Journal of Neuroscience, 53(2-4), 243-53.
49. Schandry, R., Sparrer, B., Weitkunat, R. (1986). From the heart to the brain: a study of heartbeat contingent scalp potentials. International Journal of Neuroscience, 30(4), 261-75.
50. Schandry, R., Bestler, M., Montoya, P. (1993). On the relation between cardiodynamics and heartbeat perception. Psychophysiology, 30(5), 467-74.
51. Singer, T., Critchley, H.D., Preuschoff, K. (2009). A common role of insula in feelings, empathy and uncertainty. Trends in Cognitive Science, 13(8), 334-40.
52. Stein, M.B., Simmons, A.N., Feinstein, J.S., Paulus, M.P. (2007). Increased amygdala and insula activation during emotion processing in anxiety-prone subjects. American Journal of Psychiatry, 164(2), 318-27.
53. Stormer, S.W., Heilitag, U., Knoll, J.F. (1989). Hearbeat perception and knowledge of results: a new method and some theoretical thoughts. Journal of Psychophysiology, 3(4), 340-50.
54. Thaler, L., Arnott, S.R., Goodale, M.A. (2011). Neural correlates of natural human echolocation in early and late blind echolocation experts. PLoS One, 6(5), e20162.
55. Torre-Amione, G., Southard, R.E., Loebe, M.M., et al. (2010). Reversal of secondary pulmonary hypertension by axial and pulsatile mechanical circulatory support. Journal of Heart and Lung Transplant, 29(2), 195-200.
56. Whitehead, W.E., Drescher, V.M., Heiman, P., Blackwell, B. (1977). Relation of heart rate control to heartbeat perception. Applied Psychophysiology and Biofeedback, 2(4), 371-92.
57. Wiens, S. (2005). Interoception in emotional experience. Current Opinion in Neurology, 18(4), 442-7.
58. Wiesel, T.N., Hubel, D.H. (1963). Single-cell responses in striate cortex of kittens deprived of vision in one eye. Journal of Neurophysiology, 26, 1003-17.
59. Yoder, N. (2009). PeakFinder. in http://www.mathworks.com/matlabcentral/fileexchange/25500-peakfinder (ed), Matlab, MathWorks.