Abstract
Interoception and impulsivity are two multi-dimensional constructs and although the role of interoception in impulsiveness has been previously reported, it is not clear whether their different facets are related to each other. In the present study, we aimed at bridging this gap by investigating the relationships between interoception and impulsivity in the light of their multi-dimensional nature. To this aim, we conducted a cross-task comparison and assessed in the same sample of healthy participants, interoceptive accuracy, by the heartbeat perception task, interoceptive sensibility, by a self-reported measure, “hot” impulsivity, by a behavioural task of risk taking, and “cool” impulsivity, by a go/no-go task. Also, we assessed trait impulsivity by a self-report measure. We found that interoceptive sensibility contributed to “hot” impulsivity, while interoceptive accuracy was related to non-planning trait impulsivity. These findings underscore the need to investigate at a finer grain the relationships between these two complex, multi-dimensional constructs.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bechara A, Damasio H, Tranel D, Damasio AR (1997) Deciding advantageously before knowing the advantageous strategy. Science 275:1293–1295. https://doi.org/10.1126/science.275.5304.1293
Bechara A, Tranel D, Damasio H (2000) Characterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions. Brain 123:2189–2202. https://doi.org/10.1093/brain/123.11.2189
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Statist Soc B 57:289–300. https://doi.org/10.2307/2346101
Brockett AT, Tennyson SS, deBettencourt CA, Gaye F, Roesch MR (2020) Anterior cingulate cortex is necessary for adaptation of action plans. Proc Natl Acad Sci USA 117:6196–6204. https://doi.org/10.1073/pnas.1919303117
Burnett Heyes S, Adam RJ, Urner M, van der Leer L, Bahrami B, Bays PM, Husain M (2012) Impulsivity and rapid decision-making for reward. Front Psychol 3:153. https://doi.org/10.3389/fpsyg.2012.00153
Craig AD (2002) How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 3:655–666. https://doi.org/10.1038/nrn894
Damasio AR (1996) The somatic marker hypothesis and the possible functions of the prefrontal cortex. Philos Trans R Soc Lond B Biol Sci 351:1413–1420. https://doi.org/10.1098/rstb.1996.0125
Desmedt O, Luminet O, Corneille O (2018) The heartbeat counting task largely involves non-interoceptive processes: evidence from both the original and an adapted counting task. Biol Psychol 138:185–188. https://doi.org/10.1016/j.biopsycho.2018.09.004
Desmedt O, Corneille O, Luminet O, Murphy J, Bird G, Maurage P (2020) Contribution of time estimation and knowledge to heartbeat counting task performance under original and adapted instructions. Biol Psychol 154:107904. https://doi.org/10.1016/j.biopsycho.2020.107904
Dougherty DM, Marsh DM, Mathias CW (2002) Immediate and delayed memory tasks: a computerized behavioral measure of memory, attention, and impulsivity. Behav Res Methods Instrum Comput 34:391–398. https://doi.org/10.3758/bf03195467
Erdfelder E, Faul F, Lang AG, Buchner A (2007) GPOWER: a general power analysis program. Behav Res Methods 28:1–11. https://doi.org/10.3758/BF03193146
Eysenck HJ, Eysenck MW (1985) Personality and individual differences: a natural science approach, 1st edn. Plenum Press, New York
Fossati A, Di Ceglie A, Aquarini E, Barratt ES (2001) Psychometric properties of an Italian version of the Barratt Impulsiveness Scale-11 (BIS-11) in nonclinical subjects. J Clin Psychol 57:815–828. https://doi.org/10.1002/jclp.105
Frost R, McNaughton N (2017) The neural basis of delay discounting: a review and preliminary model. Neurosci Biobehav Rev 79:48–65. https://doi.org/10.1016/j.neubiorev.2017.04.022
Fukushima H, Terasawa Y, Umeda S (2011) Association between interoception and empathy: evidence from heartbeat-evoked brain potential. Int J Psychophysiol 79:259–265. https://doi.org/10.1016/j.ijpsycho.2010.10.015
Garfinkel SN, Seth AK, Barrett AB, Suzuki K, Critchley HD (2015) Knowing your own heart: distinguishing interoceptive accuracy from interoceptive awareness. Biol Psychol 104:65–74. https://doi.org/10.1016/j.biopsycho.2014.11.004
Goel V, Dolan RJ (2003) Reciprocal neural response within lateral and ventral medial prefrontal cortex during hot and cold reasoning. Neuroimage 20:2314–2321. https://doi.org/10.1016/j.neuroimage.2003.07.027
Griffin A, Freeman LK, Trull TJ (2020) Measuring impulsivity in daily life: a systematic review and recommendations for future research. PsyArXiv. https://doi.org/10.31234/osf.io/mfdp6 ((pre-print))
Herman AM, Critchley HD, Duka T (2018a) The role of emotions and physiological arousal in modulating impulsive behaviour. Biol Psychol 133:30–43. https://doi.org/10.1016/j.biopsycho.2018.01.014
Herman AM, Critchley HD, Duka T (2018b) Risk-taking and impulsivity: the role of mood states and interoception. Front Psychol 9:1625. https://doi.org/10.3389/fpsyg.2018.01625
Herman AM, Rae CL, Critchley HD, Duka T (2019) Interoceptive accuracy predicts nonplanning trait impulsivity. Psychophysiology 56:e13339. https://doi.org/10.1111/psyp.13339
Jakubczyk A, Skrzeszewski J, Trucco EM, Suszek H, Zaorska J, Nowakowska M, Michalska A, Wojnar M, Kopera M (2019) Interoceptive accuracy and interoceptive sensibility in individuals with alcohol use disorder-different phenomena with different clinical correlations? Drug Alcohol Depend 198:34–38. https://doi.org/10.1016/j.drugalcdep.2019.01.036
Kaufmann T, Sütterlin S, Schulz S, Vögele C (2011) ARTiiFACT: a tool for heart rate artifact processing and heart rate variability analysis. Behav Res Methods 43:1161–1170. https://doi.org/10.3758/s13428-011-0107-7
Kim S, Lee D (2011) Prefrontal cortex and impulsive decision making. Biol Psychiatry 69:1140–1146. https://doi.org/10.1016/j.biopsych.2010.07.005
Knoll JF, Hodapp V (1992) A comparison between two methods for assessing heartbeat perception. Psychophysiology 29:218–222. https://doi.org/10.1111/j.1469-8986.1992.tb01689.x
Lejuez CW, Read JP, Kahler CW, Richards JB, Ramsey SE, Stuart GL, Strong DR, Brown RA (2002) Evaluation of a behavioral measure of risk taking: the Balloon Analogue Risk Task (BART). J Exp Psychol Appl 8:75–84. https://doi.org/10.1037//1076-898x.8.2.75
Longarzo M, D’Olimpio F, Chiavazzo A, Santangelo G, Trojano L, Grossi D (2015) The relationship between interoception and alexithymic trait. The self- awareness questionnaire in healthy subjects. Front Psychol 6:1149. https://doi.org/10.3389/fpsyg.2015.01149
Madden GJ, Petry NM, Johnson PS (2009) Pathological gamblers discount probabilistic rewards less steeply than matched controls. Exp Clin Psychopharmacol 17:283–290. https://doi.org/10.1037/a0016806
Mathôt S, Schreij D, Theeuwes J (2012) OpenSesame: An open-source, graphical experiment builder for the social sciences. Behav Res Methods 44:314–324. https://doi.org/10.3758/s13428-011-0168-7
Moeller FG, Barratt ES, Dougherty DM, Schmitz JM, Swann AC (2001) Psychiatric aspects of impulsivity. Am J Psychiatry 158:1783–1793. https://doi.org/10.1176/appi.ajp.158.11.1783
Moreno M, Estevez AF, Zaldivar F, Montes JMG, Gutierrez-Ferre VE, Esteban L, Sanchez-Santed F, Flores P (2012) Impulsivity differences in recreational cannabis users and binge drinkers in a university population. Drug Alcohol Depend 124:355–362. https://doi.org/10.1016/j.drugalcdep.2012.02.011
Naqvi NH, Bechara A (2010) The insula and drug addiction: an interoceptive view of pleasure, urges, and decision-making. Brain Struct Funct 214:435–450. https://doi.org/10.1007/s00429-010-0268-7
Patton JH, Stanford MS, Barratt ES (1995) Factor structure of the barratt impulsiveness scale. J Clinl Psychol 51:768–774. https://doi.org/10.1002/1097-4679(199511)51:6%3c768
Pollatos O, Gramann K, Schandry R (2007) Neural systems connecting interoceptive awareness and feelings. Hum Brain Mapp 28:9–18. https://doi.org/10.1002/hbm.20258
Pollatos O, Traut-Mattausch E, Schandry R (2009) Differential effects of anxiety and depression on interoceptive accuracy. Depress Anxiety 26:167–173. https://doi.org/10.1002/da.20504
Quadt L, Critchley HD, Garfinkel SN (2018) The neurobiology of interoception in health and disease. Ann NY Acad Sci 1428:112–128. https://doi.org/10.1111/nyas.13915
Rae CL, Larsson DEO, Garfinkel SN, Critchley HD (2019) Dimensions of interoception predict premonitory urges and tic severity in Tourette syndrome. Psychiatry Res 271:469–475. https://doi.org/10.1016/j.psychres.2018.12.036
Rae CL, Ahmad A, Larsson DEO, Silva M, Praag CDGV, Garfinkel SN, Critchley HD (2020) Impact of cardiac interoception cues and confidence on voluntary decisions to make or withhold action in an intentional inhibition task. Sci Rep 10:4184. https://doi.org/10.1038/s41598-020-60405-8
Rao H, Korczykowski M, Pluta J, Hoang A, Detre JA (2008) Neural correlates of voluntary and involuntary risk taking in the human brain: An fMRI study of the Balloon Analog Risk Task (BART). Neuroimage 42:902–910. https://doi.org/10.1016/j.neuroimage.2008.05.046
Ring C, Brener J (2018) Heartbeat counting is unrelated to heartbeat detection: a comparison of methods to quantify interoception. Psichophysiology 55:e13084. https://doi.org/10.1111/psyp.13084
Rubia K (2011) “Cool” inferior frontostriatal dysfunction in attention-deficit/hyperactivity disorder versus “hot” ventromedial orbitofrontal-limbic dysfunction in conduct disorder: a review. Biol Psychiatry 15:e69-87. https://doi.org/10.1016/j.biopsych.2010.09.023
Salvato G, De Maio G, Bottini G (2019) Interoceptive sensibility tunes risk-taking behaviour when body-related stimuli come into play. Sci Rep 20(9):2396. https://doi.org/10.1038/s41598-019-39061-0
Santangelo G, Vitale C, Baiano C, D’Iorio A, Longo K, Barone P, Amboni M, Conson M (2018) Interoceptive processing deficit: a behavioral marker for subtyping Parkinson’s disease. Parkinsonism Relat Disord 53:64–69. https://doi.org/10.1016/j.parkreldis.2018.05.001
Schandry R (1981) Heartbeat perception and emotional experience. Psychophysiology 18:483–488. https://doi.org/10.1111/j.1469-8986.1981.tb02486.x
Sellitto M, Ciaramelli E, Mattioli F, di Pellegrino G (2016) Reduced sensitivity to sooner reward during intertemporal decision-making following insula damage in humans. Front Behav Neurosci. https://doi.org/10.3389/fnbeh.2015.00367
Shah P, Hall R, Catmur C, Bird G (2016) Alexithymia, not autism, is associated with impaired interoception. Cortex 81:215–220. https://doi.org/10.1016/j.cortex.2016.03.021
Teghil A, Boccia M, Nocera L, Pietranelli V, Guariglia C (2020) Interoceptive awareness selectively predicts timing accuracy in irregular contexts. Behav Brain Res 377:112242. https://doi.org/10.1016/j.bbr.2019.112242
Werner NS, Jung K, Duschek S, Schandry R (2009) Enhanced cardiac perception is associated with benefits in decision-making. Psychophysiology 46:1123–1129. https://doi.org/10.1111/j.1469-8986.2009.00855.x
Wessel JR (2018) Prepotent motor activity and inhibitory control demands in different variants of the go/no-go paradigm. Psychophysiology. https://doi.org/10.1111/psyp.12871
White TL, Lejuez CW, de Wit H (2008) Test-retest characteristics of the Balloon Analogue Risk Task (BART). Exp Clin Psychopharmacol 16:565–570. https://doi.org/10.1037/a0014083
Funding
No funding was received.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Availability of data and material (data transparency)
The data are available by writing an email to corresponding author.
Additional information
Communicated by Bill J Yates.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Baiano, C., Santangelo, G., Senese, V.P. et al. Linking perception of bodily states and cognitive control: the role of interoception in impulsive behaviour. Exp Brain Res 239, 857–865 (2021). https://doi.org/10.1007/s00221-020-06022-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-020-06022-3