Altered neural signatures of interoception in multiple sclerosis

Multiple sclerosis (MS) patients present several alterations related to sensing of bodily signals. However, no specific neurocognitive impairment has yet been proposed as a core deficit underlying such symptoms. We aimed to determine whether MS patients present changes in interoception—that is, the...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autor principal: Salamone, P.C
Otros Autores: Esteves, S., Sinay, V.J, García-Cordero, I., Abrevaya, S., Couto, B., Adolfi, F., Martorell, M., Petroni, A., Yoris, A., Torquati, K., Alifano, F., Legaz, A., Cassará, F.P, Bruno, D., Kemp, A.H, Herrera, E., García, A.M, Ibáñez, A., Sedeño, L.
Formato: Capítulo de libro
Lenguaje:Inglés
Publicado: John Wiley and Sons Inc. 2018
Acceso en línea:Registro en Scopus
DOI
Handle
Registro en la Biblioteca Digital
Aporte de:Registro referencial: Solicitar el recurso aquí
Descripción
Sumario:Multiple sclerosis (MS) patients present several alterations related to sensing of bodily signals. However, no specific neurocognitive impairment has yet been proposed as a core deficit underlying such symptoms. We aimed to determine whether MS patients present changes in interoception—that is, the monitoring of autonomic bodily information—a process that might be related to various bodily dysfunctions. We performed two studies in 34 relapsing–remitting, early-stage MS patients and 46 controls matched for gender, age, and education. In Study 1, we evaluated the heartbeat-evoked potential (HEP), a cortical signature of interoception, via a 128-channel EEG system during a heartbeat detection task including an exteroceptive and an interoceptive condition. Then, we obtained whole-brain MRI recordings. In Study 2, participants underwent fMRI recordings during two resting-state conditions: mind wandering and interoception. In Study 1, controls exhibited greater HEP modulation during the interoceptive condition than the exteroceptive one, but no systematic differences between conditions emerged in MS patients. Patients presented atrophy in the left insula, the posterior part of the right insula, and the right anterior cingulate cortex, with abnormal associations between neurophysiological and neuroanatomical patterns. In Study 2, controls showed higher functional connectivity and degree for the interoceptive state compared with mind wandering; however, this pattern was absent in patients, who nonetheless presented greater connectivity and degree than controls during mind wandering. MS patients were characterized by atypical multimodal brain signatures of interoception. This finding opens a new agenda to examine the role of inner-signal monitoring in the body symptomatology of MS. © 2018 Wiley Periodicals, Inc.
Bibliografía:Adolfi, F., Couto, B., Richter, F., Decety, J., Lopez, J., Sigman, M., Ibanez, A., Convergence of interoception, emotion, and social cognition: A twofold fMRI meta-analysis and lesion approach (2017) Cortex, 88, pp. 124-142. , https://doi.org/10.1016/j.cortex.2016.12.019
Amoruso, L., Sedeno, L., Huepe, D., Tomio, A., Kamienkowski, J., Hurtado, E., Ibanez, A., Time to tango: Expertise and contextual anticipation during action observation (2014) NeuroImage, 98, pp. 366-385. , https://doi.org/10.1016/j.neuroimage.2014.05.005
Ashburner, J., A fast diffeomorphic image registration algorithm (2007) NeuroImage, 38 (1), pp. 95-113. , https://doi.org/10.1016/j.neuroimage.2007.07.007
Ashburner, J., Friston, K.J., Nonlinear spatial normalization using basis functions (1999) Human Brain Mapping, 7 (4), pp. 254-266
Ashburner, J., Friston, K.J., Voxel-based morphometry--the methods (2000) NeuroImage, 11 (6), pp. 805-821. , https://doi.org/10.1006/nimg.2000.0582
Barttfeld, P., Wicker, B., Cukier, S., Navarta, S., Lew, S., Leiguarda, R., Sigman, M., State-dependent changes of connectivity patterns and functional brain network topology in autism spectrum disorder (2012) Neuropsychologia, 50 (14), pp. 3653-3662. , https://doi.org/10.1016/j.neuropsychologia.2012.09.047
Bullmore, E.T., Bassett, D.S., Brain graphs: Graphical models of the human brain connectome (2011) Annual Review of Clinical Psychology, 7, pp. 113-140. , https://doi.org/10.1146/annurev-clinpsy-040510-143934
Bullmore, E., Sporns, O., Complex brain networks: Graph theoretical analysis of structural and functional systems (2009) Nature Reviews. Neuroscience, 10 (3), pp. 186-198. , https://doi.org/10.1038/nrn2575
Canales-Johnson, A., Silva, C., Huepe, D., Rivera-Rei, A., Noreika, V., Garcia Mdel, C., Bekinschtein, T.A., Auditory feedback differentially modulates Behavioral and neural markers of objective and subjective performance when tapping to your heartbeat (2015) Cerebral Cortex, 25 (11), pp. 4490-4503. , https://doi.org/10.1093/cercor/bhv076
Chao-Gan, Y., Yu-Feng, Z., DPARSF: A MATLAB toolbox for "pipeline" data analysis of resting-state fMRI (2010) Frontiers in Systems Neuroscience, 4, p. 13. , https://doi.org/10.3389/fnsys.2010.00013
Chennu, S., Noreika, V., Gueorguiev, D., Blenkmann, A., Kochen, S., Ibanez, A., Bekinschtein, T.A., Expectation and attention in hierarchical auditory prediction (2013) The Journal of Neuroscience, 33 (27), pp. 11194-11205. , https://doi.org/10.1523/JNEUROSCI.0114-13.2013
Couto, B., Adolfi, F., Sedeno, L., Salles, A., Canales-Johnson, A., Alvarez-Abut, P., Ibanez, A., Disentangling interoception: Insights from focal strokes affecting the perception of external and internal milieus (2015) Frontiers in Psychology, 6, p. 503. , https://doi.org/10.3389/fpsyg.2015.00503
Couto, B., Adolfi, F., Velasquez, M., Mesow, M., Feinstein, J., Canales-Johnson, A., Ibanez, A., Heart evoked potential triggers brain responses to natural affective scenes: A preliminary study (2015) Autonomic Neuroscience, 193, pp. 132-137. , https://doi.org/10.1016/j.autneu.2015.06.006
Couto, B., Manes, F., Montanes, P., Matallana, D., Reyes, P., Velasquez, M., Ibanez, A., Structural neuroimaging of social cognition in progressive non-fluent aphasia and behavioral variant of frontotemporal dementia (2013) Frontiers in Human Neuroscience, 7, p. 467. , https://doi.org/10.3389/fnhum.2013.00467
Couto, B., Salles, A., Sedeno, L., Peradejordi, M., Barttfeld, P., Canales-Johnson, A., Ibanez, A., The man who feels two hearts: The different pathways of interoception (2014) Social Cognitive and Affective Neuroscience, 9 (9), pp. 1253-1260. , https://doi.org/10.1093/scan/nst108
Craig, A.D., How do you feel? Interoception: The sense of the physiological condition of the body (2002) Nature Reviews. Neuroscience, 3 (8), pp. 655-666. , https://doi.org/10.1038/nrn894
Craig, A.D., Human feelings: Why are some more aware than others? (2004) Trends in Cognitive Sciences, 8 (6), pp. 239-241. , https://doi.org/10.1016/j.tics.2004.04.004
Critchley, H.D., Harrison, N.A., Visceral influences on brain and behavior (2013) Neuron, 77 (4), pp. 624-638. , https://doi.org/10.1016/j.neuron.2013.02.008
Critchley, H.D., Wiens, S., Rotshtein, P., Ohman, A., Dolan, R.J., Neural systems supporting interoceptive awareness (2004) Nature Neuroscience, 7 (2), pp. 189-195. , https://doi.org/10.1038/nn1176
Cruz Gomez, A.J., Ventura Campos, N., Belenguer, A., Avila, C., Forn, C., Regional brain atrophy and functional connectivity changes related to fatigue in multiple sclerosis (2013) PLoS One, 8 (10). , https://doi.org/10.1371/journal.pone.0077914
Dantzer, R., Heijnen, C.J., Kavelaars, A., Laye, S., Capuron, L., The neuroimmune basis of fatigue (2014) Trends in Neurosciences, 37 (1), pp. 39-46. , https://doi.org/10.1016/j.tins.2013.10.003
Davis, S.L., Wilson, T.E., White, A.T., Frohman, E.M., Thermoregulation in multiple sclerosis (2010) Journal of Applied Physiology (1985), 109 (5), pp. 1531-1537. , https://doi.org/10.1152/japplphysiol.00460.2010
Dirlich, G., Vogl, L., Plaschke, M., Strian, F., Cardiac field effects on the EEG (1997) Electroencephalography and Clinical Neurophysiology, 102 (4), pp. 307-315
Domschke, K., Stevens, S., Pfleiderer, B., Gerlach, A.L., Interoceptive sensitivity in anxiety and anxiety disorders: An overview and integration of neurobiological findings (2010) Clinical Psychology Review, 30 (1), pp. 1-11. , https://doi.org/10.1016/j.cpr.2009.08.008
Doty, R.L., Tourbier, I.A., Pham, D.L., Cuzzocreo, J.L., Udupa, J.K., Karacali, B., Yousem, D.M., Taste dysfunction in multiple sclerosis (2016) Journal of Neurology, 263 (4), pp. 677-688. , https://doi.org/10.1007/s00415-016-8030-6
Faivre, A., Rico, A., Zaaraoui, W., Crespy, L., Reuter, F., Wybrecht, D., Audoin, B., Assessing brain connectivity at rest is clinically relevant in early multiple sclerosis (2012) Multiple Sclerosis, 18 (9), pp. 1251-1258. , https://doi.org/10.1177/1352458511435930
Farb, N.A., Segal, Z.V., Anderson, A.K., Attentional modulation of primary interoceptive and exteroceptive cortices (2013) Cerebral Cortex, 23 (1), pp. 114-126. , https://doi.org/10.1093/cercor/bhr385
Filippi, M., Agosta, F., Spinelli, E.G., Rocca, M.A., Imaging resting state brain function in multiple sclerosis (2013) Journal of Neurology, 260 (7), pp. 1709-1713. , https://doi.org/10.1007/s00415-012-6695-z
Fox, M.D., Snyder, A.Z., Vincent, J.L., Corbetta, M., Van Essen, D.C., Raichle, M.E., The human brain is intrinsically organized into dynamic, anticorrelated functional networks (2005) Proceedings of the National Academy of Sciences of the United States of America, 102 (27), pp. 9673-9678. , https://doi.org/10.1073/pnas.0504136102
Fukushima, H., Terasawa, Y., Umeda, S., Association between interoception and empathy: Evidence from heartbeat-evoked brain potential (2011) International Journal of Psychophysiology, 79 (2), pp. 259-265. , https://doi.org/10.1016/j.ijpsycho.2010.10.015
Garcia-Cordero, I., Esteves, S., Mikulan, E.P., Hesse, E., Baglivo, F.H., Silva, W., Sedeno, L., Attention, in and out: Scalp-level and intracranial EEG correlates of Interoception and Exteroception (2017) Frontiers in Neuroscience, 11, p. 411. , https://doi.org/10.3389/fnins.2017.00411
Garcia-Cordero, I., Sedeno, L., de la Fuente, L., Slachevsky, A., Forno, G., Klein, F., Ibanez, A., Feeling, learning from and being aware of inner states: Interoceptive dimensions in neurodegeneration and stroke (2016) Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 371 (1708), p. 20160006. , https://doi.org/10.1098/rstb.2016.0006
Garfinkel, S.N., Seth, A.K., Barrett, A.B., Suzuki, K., Critchley, H.D., Knowing your own heart: Distinguishing interoceptive accuracy from interoceptive awareness (2015) Biological Psychology, 104, pp. 65-74. , https://doi.org/10.1016/j.biopsycho.2014.11.004
Gonzalez-Gadea, M.L., Chennu, S., Bekinschtein, T.A., Rattazzi, A., Beraudi, A., Tripicchio, P., Ibanez, A., Predictive coding in autism spectrum disorder and attention deficit hyperactivity disorder (2015) Journal of Neurophysiology, 114 (5), pp. 2625-2636. , https://doi.org/10.1152/jn.00543.2015
Good, C.D., Johnsrude, I.S., Ashburner, J., Henson, R.N., Friston, K.J., Frackowiak, R.S., A voxel-based morphometric study of ageing in 465 normal adult human brains (2001) NeuroImage, 14 (1), pp. 21-36. , https://doi.org/10.1006/nimg.2001.0786
Gramsch, C., Kattoor, J., Icenhour, A., Forsting, M., Schedlowski, M., Gizewski, E.R., Elsenbruch, S., Learning pain-related fear: Neural mechanisms mediating rapid differential conditioning, extinction and reinstatement processes in human visceral pain (2014) Neurobiology of Learning and Memory, 116, pp. 36-45. , https://doi.org/10.1016/j.nlm.2014.08.003
Hanken, K., Eling, P., Hildebrandt, H., The representation of inflammatory signals in the brain - a model for subjective fatigue in multiple sclerosis (2014) Frontiers in Neurology, 5, p. 264. , https://doi.org/10.3389/fneur.2014.00264
He, Y., Dagher, A., Chen, Z., Charil, A., Zijdenbos, A., Worsley, K., Evans, A., Impaired small-world efficiency in structural cortical networks in multiple sclerosis associated with white matter lesion load (2009) Brain, 132, pp. 3366-3379. , https://doi.org/10.1093/brain/awp089
Ibanez, A., Cardona, J.F., Dos Santos, Y.V., Blenkmann, A., Aravena, P., Roca, M., Bekinschtein, T., Motor-language coupling: Direct evidence from early Parkinson's disease and intracranial cortical recordings (2013) Cortex, 49 (4), pp. 968-984. , https://doi.org/10.1016/j.cortex.2012.02.014
Irish, M., Piguet, O., Hodges, J.R., Hornberger, M., Common and unique gray matter correlates of episodic memory dysfunction in frontotemporal dementia and Alzheimer's disease (2014) Human Brain Mapping, 35 (4), pp. 1422-1435. , https://doi.org/10.1002/hbm.22263
Katkin, E.S., Cestaro, V.L., Weitkunat, R., Individual differences in cortical evoked potentials as a function of heartbeat detection ability (1991) The International Journal of Neuroscience, 61 (3-4), pp. 269-276
Khalsa, S.S., Rudrauf, D., Feinstein, J.S., Tranel, D., The pathways of interoceptive awareness (2009) Nature Neuroscience, 12 (12), pp. 1494-1496. , https://doi.org/10.1038/nn.2411
Kim, D., Kim, S.K., Comparing patterns of component loadings: Principal component analysis (PCA) versus independent component analysis (ICA) in analyzing multivariate non-normal data (2012) Behavior Research Methods, 44 (4), pp. 1239-1243. , https://doi.org/10.3758/s13428-012-0193-1
Kluckow, S.W., Rehbein, J.G., Schwab, M., Witte, O.W., Bublak, P., What you get from what you see: Parametric assessment of visual processing capacity in multiple sclerosis and its relation to cognitive fatigue (2016) Cortex, 83, pp. 167-180. , https://doi.org/10.1016/j.cortex.2016.07.018
Kruczyk, M., Umer, H.M., Enroth, S., Komorowski, J., Peak finder Metaserver - a novel application for finding peaks in ChIP-seq data (2013) BMC Bioinformatics, 14, p. 280. , https://doi.org/10.1186/1471-2105-14-280
Krupp, L., Fatigue is intrinsic to multiple sclerosis (MS) and is the most commonly reported symptom of the disease (2006) Multiple Sclerosis, 12 (4), pp. 367-368
Kurth, F., Zilles, K., Fox, P.T., Laird, A.R., Eickhoff, S.B., A link between the systems: Functional differentiation and integration within the human insula revealed by meta-analysis (2010) Brain Structure & Function, 214 (5-6), pp. 519-534. , https://doi.org/10.1007/s00429-010-0255-z
Kurtzke, J.F., Rating neurologic impairment in multiple sclerosis: An expanded disability status scale (EDSS) (1983) Neurology, 33 (11), pp. 1444-1452
Lansley, J., Mataix-Cols, D., Grau, M., Radua, J., Sastre-Garriga, J., Localized grey matter atrophy in multiple sclerosis: A meta-analysis of voxel-based morphometry studies and associations with functional disability (2013) Neuroscience and Biobehavioral Reviews, 37 (5), pp. 819-830. , https://doi.org/10.1016/j.neubiorev.2013.03.006
Manly, B.F., (2006) Randomization, bootstrap and Monte Carlo methods in biology, , Boca Raton, FL, CRC Press
Melloni, M., Billeke, P., Baez, S., Hesse, E., de la Fuente, L., Forno, G., Ibanez, A., Your perspective and my benefit: Multiple lesion models of self-other integration strategies during social bargaining (2016) Brain, 139, pp. 3022-3040. , https://doi.org/10.1093/brain/aww231
Melloni, M., Sedeno, L., Hesse, E., Garcia-Cordero, I., Mikulan, E., Plastino, A., Ibanez, A., Cortical dynamics and subcortical signatures of motor-language coupling in Parkinson's disease (2015) Scientific Reports, 5, p. 11899. , https://doi.org/10.1038/srep11899
Michal, M., Reuchlein, B., Adler, J., Reiner, I., Beutel, M.E., Vogele, C., Schulz, A., Striking discrepancy of anomalous body experiences with normal interoceptive accuracy in depersonalization-derealization disorder (2014) PLoS One, 9 (2). , https://doi.org/10.1371/journal.pone.0089823
Michalski, D., Liebig, S., Thomae, E., Hinz, A., Bergh, F.T., Pain in patients with multiple sclerosis: A complex assessment including quantitative and qualitative measurements provides for a disease-related biopsychosocial pain model (2011) Journal of Pain Research, 4, pp. 219-225. , https://doi.org/10.2147/JPR.S20309
Montoya, P., Schandry, R., Muller, A., Heartbeat evoked potentials (HEP): Topography and influence of cardiac awareness and focus of attention (1993) Electroencephalography and Clinical Neurophysiology, 88 (3), pp. 163-172
Muller, L.E., Schulz, A., Andermann, M., Gabel, A., Gescher, D.M., Spohn, A., Bertsch, K., Cortical representation of afferent bodily signals in borderline personality disorder: Neural correlates and relationship to emotional Dysregulation (2015) JAMA Psychiatry, 72 (11), pp. 1077-1086. , https://doi.org/10.1001/jamapsychiatry.2015.1252
Nichols, T.E., Das, S., Eickhoff, S.B., Evans, A.C., Glatard, T., Hanke, M., Yeo, B.T., Best practices in data analysis and sharing in neuroimaging using MRI (2017) Nature Neuroscience, 20 (3), pp. 299-303. , https://doi.org/10.1038/nn.4500
Pardini, M., Bonzano, L., Bergamino, M., Bommarito, G., Feraco, P., Murugavel, A., Roccatagliata, L., Cingulum bundle alterations underlie subjective fatigue in multiple sclerosis (2015) Multiple Sclerosis, 21 (4), pp. 442-447. , https://doi.org/10.1177/1352458514546791
Poldrack, R.A., Baker, C.I., Durnez, J., Gorgolewski, K.J., Matthews, P.M., Munafo, M.R., Yarkoni, T., Scanning the horizon: Toward transparent and reproducible neuroimaging research (2017) Nature Reviews. Neuroscience, 18 (2), pp. 115-126. , https://doi.org/10.1038/nrn.2016.167
Polman, C.H., Reingold, S.C., Banwell, B., Clanet, M., Cohen, J.A., Filippi, M., Wolinsky, J.S., Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria (2011) Annals of Neurology, 69 (2), pp. 292-302. , https://doi.org/10.1002/ana.22366
Pollatos, O., Kirsch, W., Schandry, R., Brain structures involved in interoceptive awareness and cardioafferent signal processing: A dipole source localization study (2005) Human Brain Mapping, 26 (1), pp. 54-64. , https://doi.org/10.1002/hbm.20121
Pollatos, O., Schandry, R., Accuracy of heartbeat perception is reflected in the amplitude of the heartbeat-evoked brain potential (2004) Psychophysiology, 41 (3), pp. 476-482
Raichle, M.E., A paradigm shift in functional brain imaging (2009) The Journal of Neuroscience, 29 (41), pp. 12729-12734. , https://doi.org/10.1523/JNEUROSCI.4366-09.2009
Rocca, M.A., Amato, M.P., De Stefano, N., Enzinger, C., Geurts, J.J., Penner, I.K., Filippi, M., Clinical and imaging assessment of cognitive dysfunction in multiple sclerosis (2015) Lancet Neurology, 14 (3), pp. 302-317. , https://doi.org/10.1016/S1474-4422(14)70250-9
Rocca, M.A., Valsasina, P., Martinelli, V., Misci, P., Falini, A., Comi, G., Filippi, M., Large-scale neuronal network dysfunction in relapsing-remitting multiple sclerosis (2012) Neurology, 79 (14), pp. 1449-1457. , https://doi.org/10.1212/WNL.0b013e31826d5f10
Roosendaal, S.D., Schoonheim, M.M., Hulst, H.E., Sanz-Arigita, E.J., Smith, S.M., Geurts, J.J., Barkhof, F., Resting state networks change in clinically isolated syndrome (2010) Brain, 133, pp. 1612-1621. , https://doi.org/10.1093/brain/awq058
Roxburgh, R.H., Seaman, S.R., Masterman, T., Hensiek, A.E., Sawcer, S.J., Vukusic, S., Compston, D.A., Multiple sclerosis severity score: Using disability and disease duration to rate disease severity (2005) Neurology, 64 (7), pp. 1144-1151. , https://doi.org/10.1212/01.WNL.0000156155.19270.F8
Rubinov, M., Sporns, O., Complex network measures of brain connectivity: Uses and interpretations (2010) NeuroImage, 52 (3), pp. 1059-1069. , https://doi.org/10.1016/j.neuroimage.2009.10.003
Schandry, R., Montoya, P., Event-related brain potentials and the processing of cardiac activity (1996) Biological Psychology, 42 (1-2), pp. 75-85
Schandry, R., Weitkunat, R., Enhancement of heartbeat-related brain potentials through cardiac awareness training (1990) The International Journal of Neuroscience, 53 (2-4), pp. 243-253
Schulz, A., Koster, S., Beutel, M.E., Schachinger, H., Vogele, C., Rost, S., Michal, M., Altered patterns of heartbeat-evoked potentials in depersonalization/derealization disorder: Neurophysiological evidence for impaired cortical representation of bodily signals (2015) Psychosomatic Medicine, 77 (5), pp. 506-516. , https://doi.org/10.1097/PSY.0000000000000195
Schulz, S.M., Neural correlates of heart-focused interoception: A functional magnetic resonance imaging meta-analysis (2016) Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 371 (1708), p. 20160018. , https://doi.org/10.1098/rstb.2016.0018
Sedeno, L., Couto, B., Melloni, M., Canales-Johnson, A., Yoris, A., Baez, S., Ibanez, A., How do you feel when you can't feel your body? Interoception, functional connectivity and emotional processing in depersonalization-derealization disorder (2014) PLoS One, 9 (6). , https://doi.org/10.1371/journal.pone.0098769
Shao, S., Shen, K., Wilder-Smith, E.P., Li, X., Effect of pain perception on the heartbeat evoked potential (2011) Clinical Neurophysiology, 122 (9), pp. 1838-1845. , https://doi.org/10.1016/j.clinph.2011.02.014
Silva, A.M., Santos, E., Moreira, I., Bettencourt, A., Coutinho, E., Goncalves, A., Cavaco, S., Olfactory dysfunction in multiple sclerosis: Association with secondary progression (2012) Multiple Sclerosis, 18 (5), pp. 616-621. , https://doi.org/10.1177/1352458511427156
Simmons, W.K., Avery, J.A., Barcalow, J.C., Bodurka, J., Drevets, W.C., Bellgowan, P., Keeping the body in mind: Insula functional organization and functional connectivity integrate interoceptive, exteroceptive, and emotional awareness (2013) Human Brain Mapping, 34 (11), pp. 2944-2958. , https://doi.org/10.1002/hbm.22113
Terhaar, J., Viola, F.C., Bar, K.J., Debener, S., Heartbeat evoked potentials mirror altered body perception in depressed patients (2012) Clinical Neurophysiology, 123 (10), pp. 1950-1957. , https://doi.org/10.1016/j.clinph.2012.02.086
Tsakiris, M., Tajadura-Jimenez, A., Costantini, M., Just a heartbeat away from one's body: Interoceptive sensitivity predicts malleability of body-representations (2011) Proceedings of the Biological Sciences, 278 (1717), pp. 2470-2476. , https://doi.org/10.1098/rspb.2010.2547
Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., Joliot, M., Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain (2002) NeuroImage, 15 (1), pp. 273-289. , https://doi.org/10.1006/nimg.2001.0978
Vercoulen, J.H., Hommes, O.R., Swanink, C.M., Jongen, P.J., Fennis, J.F., Galama, J.M., Bleijenberg, G., The measurement of fatigue in patients with multiple sclerosis. A multidimensional comparison with patients with chronic fatigue syndrome and healthy subjects (1996) Archives of Neurology, 53 (7), pp. 642-649
Weitkunat, R., Motivation and heartbeat evoked potentials (1990) Psychophysiology, 4, pp. 33-40
Yoris, A., Abrevaya, S., Esteves, S., Salamone, P., Lori, N., Martorell, M., Ibanez, A., Multilevel convergence of interoceptive impairments in hypertension: New evidence of disrupted body-brain interactions (2018) Human Brain Mapping, 39 (4), pp. 1563-1581. , https://doi.org/10.1002/hbm.23933
Yoris, A., Esteves, S., Couto, B., Melloni, M., Kichic, R., Cetkovich, M., Sedeno, L., The roles of interoceptive sensitivity and metacognitive interoception in panic (2015) Behavioral and Brain Functions, 11, p. 14. , https://doi.org/10.1186/s12993-015-0058-8
Yoris, A., García, A., Traiber, L., Santamaría-García, H., Esteves, S., Martorell, M., Sedeno, L., The inner world of overactive monitoring: Neural markers of interoception in OCD (2017) Psychological Medicine, 47, pp. 1957-1970
Yoris, A., García, A.M., Salamone, P., Sedeno, L., García-Cordero, I., Ibanez, A., Cardiac interoception in neurological conditions and its relevance for dimensional approaches (2018) The Interoceptive Basis of the Mind, , M. Tsakiris, &, H. E. De Preester, (Eds.),, Oxford, UK, Oxford University Press
Yoris, A., Garcia, A.M., Traiber, L., Santamaria-Garcia, H., Martorell, M., Alifano, F., Sedeno, L., The inner world of overactive monitoring: Neural markers of interoception in obsessive-compulsive disorder (2017) Psychological Medicine, 47 (11), pp. 1957-1970. , https://doi.org/10.1017/S0033291717000368
Yuan, H., Yan, H.M., Xu, X.G., Han, F., Yan, Q., Effect of heartbeat perception on heartbeat evoked potential waves (2007) Neuroscience Bulletin, 23 (6), pp. 357-362. , https://doi.org/10.1007/s12264-007-0053-7
ISSN:10659471
DOI:10.1002/hbm.24319