Skip to main content Accessibility help
×
Hostname: page-component-76fb5796d-x4r87 Total loading time: 0 Render date: 2024-04-29T22:50:04.428Z Has data issue: false hasContentIssue false

Chapter 6 - Interoceptive Integration in the Primate Insular Cortex

from Section 1 - The Human Insula from an Epileptological Standpoint

Published online by Cambridge University Press:  09 June 2022

Dang Nguyen
Affiliation:
Université de Montréal
Jean Isnard
Affiliation:
Claude Bernard University Lyon
Philippe Kahane
Affiliation:
Grenoble-Alpes University Hospital
Get access

Summary

The functional organization of the primate insula is shaped by interoceptive afferents encoding ongoing homeostatic bodily states. A differential posterior, middle, and anterior integration of these afferents with somatomotor, environmental, autonomic, and hedonic activities has been proposed to culminate in an ultimate representation of subjective feelings in the anterior insula in humans. Recent examinations of the insula in macaque monkeys indicate that such integration could occur within a consistent postero-anterior and dorso-ventral latticework pattern. The disproportionate expansion of the anterior insula in humans could have been accompanied by an enrichment of high-order homeostatic representations associated with motoric and autonomic efferent output and with the descriptively less distinct but arousing sensations underlying subjective feelings.

Type
Chapter
Information
Insular Epilepsies , pp. 52 - 66
Publisher: Cambridge University Press
Print publication year: 2022

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Craig, AD. How do you feel? Interoception: The sense of the physiological condition of the body. Nature Rev Neurosci. 2002 Aug;3(8):655666.Google Scholar
Craig, AD. How Do You Feel? An Interoceptive Moment with Your Neurobiological Self: Princeton University Press; 2015.CrossRefGoogle Scholar
Craig, AD. How do you feel – now? The anterior insula and human awareness. Nature Rev Neurosci. 2009 Jan;10(1):5970.CrossRefGoogle Scholar
Evrard, HC. Organization of the primate insular cortex. Front Neuroanat. 2019;8:1343.Google Scholar
Johnson, JI, Buchanan, KJ, Morris, JA, Fobbs, AJ, editors. Interrelation of gyral formations, cytoarchitectural variations, and sensory regions in human insular cortex. Soc Neurosci (Online); 2009.Google Scholar
Wysiadecki, G, Malkiewicz, A, Rozniecki, J, Polguj, M, Haladaj, R, Zytkowski, A, et al. Anatomical variations of the insular gyri: A morphological study and proposal of unified classification. Clin Anat. 2018 Apr;31(3):347356.CrossRefGoogle ScholarPubMed
Allman, JM, Tetreault, NA, Hakeem, AY, Manaye, KF, Semendeferi, K, Erwin, JM, et al. The von Economo neurons in frontoinsular and anterior cingulate cortex in great apes’ and humans’ brain. Structure & Function. 2010 Jun;214(5–6):495517.Google Scholar
Evrard, HC, Forro, T, Logothetis, NK. Von Economo neurons in the anterior insula of the macaque monkey. Neuron. 2012;74:482489.Google Scholar
Evrard, HC, Logothetis, NK, Craig, AD. Modular architectonic organization of the insula in the macaque monkey. Journal of Comparative Neurology. 2014 Jul 31;522:6497.Google Scholar
Kurth, F, Eickhoff, SB, Schleicher, A, Hoemke, L, Zilles, K, Amunts, K. Cytoarchitecture and probabilistic maps of the human posterior insular cortex. Cerebral Cortex. 2010 Jun;20(6):14481461.Google Scholar
Bauernfeind, AL, de Sousa, AA, Avasthi, T, Dobson, SD, Raghanti, MA, Lewandowski, AH, et al. A volumetric comparison of the insular cortex and its subregions in primates. Journal of Human Evolution. 2013 Apr;64(4):263279.CrossRefGoogle ScholarPubMed
Horn, FM, Evrard, HC, editors. Multiple areal distributions of the von Economo and fork neurons in the human anterior insular cortex. 49th Annual Meeting of the Society for Neuroscience; 2018; San Diego.Google Scholar
Harrison, NA, Gray, MA, Gianaros, PJ, Critchley, HD. The embodiment of emotional feelings in the brain. Journal of Neuroscience. 2010 Sep 22;30(38):1287812884.CrossRefGoogle ScholarPubMed
Critchley, H, Garfinkel, SN. The influence of physiological signals on cognition Curr Op Behav Sci. 2018;19:1318.Google Scholar
Prechtl, JC, Powell TP. B-Afferents: A fundamental division of the nervous system mediating hoxneostasis? Behav Brain Sci. 1990;13:289331.CrossRefGoogle Scholar
Craig, AD. Distribution of brainstem projections from spinal lamina I neurons in the cat and the monkey Journal of Comparative Neurology. 1995 Oct 16;361(2):225248.CrossRefGoogle Scholar
Boscan, P, Pickering, AE, Paton, JF. The nucleus of the solitary tract: an integrating station for nociceptive and cardiorespiratory afferents. Experimental Physiology. 2002 Mar;87(2):259266.Google Scholar
Beckstead, RM, Morse, JR, Norgren, R. The nucleus of the solitary tract in the monkey: projections to the thalamus and brain stem nuclei. Journal of Comparative Neurology. 1980 Mar 15;190(2):259282.CrossRefGoogle Scholar
Craig, AD. Distribution of trigeminothalamic and spinothalamic lamina I terminations in the macaque monkey. Journal of Comparative Neurology. 2004 Sep 13;477(2):119148.Google Scholar
Chien, JH, Korzeniewska, A, Colloca, L, Campbell, C, Dougherty, P, Lenz, F. Human thalamic somatosensory nucleus (ventral caudal, Vc) as a locus for stimulation by inputs from tactile, noxious and thermal sensors on active prosthesis sensors. Sensors. 2017 May 24;17(6):11971213.CrossRefGoogle Scholar
Vartiainen, N, Perchet, C, Magnin, M, Creac’h, C, Convers, P, Nighoghossian, N, et al. Thalamic pain: Anatomical and physiological indices of prediction. Brain. 2016 Mar;139(pt 3):708722.Google Scholar
Dum, RP, Levinthal, DJ, Strick, PL. The spinothalamic system targets motor and sensory areas in the cerebral cortex of monkeys. Journal of Neuroscience. 2009 Nov 11;29(45):1422314235.CrossRefGoogle ScholarPubMed
Strigo, IA, Craig, AD. Interoception, homeostatic emotions and sympathovagal balance. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences. 2016 Nov 19;371(1708).Google Scholar
Blomqvist, A, Zhang, ET, Craig, AD. Cytoarchitectonic and immunohistochemical characterization of a specific pain and temperature relay, the posterior portion of the ventral medial nucleus, in the human thalamus. Brain. 2000 Mar;123(pt 3):601619.Google Scholar
Pritchard, TC, Hamilton, RB, Norgren, R. Projections of the parabrachial nucleus in the old world monkey. Experimental Neurology. 2000 Sep;165(1):101117.Google Scholar
Lenz, FA, Gracely, RH, Zirh, TA, Leopold, DA, Rowland, LH, Dougherty, PM. Human thalamic nucleus mediating taste and multiple other sensations related to ingestive behavior. Journal of Neurophysiology. 1997 Jun;77(6):34063409.Google Scholar
Pritchard, TC, Hamilton, RB, Norgren, R. Neural coding of gustatory information in the thalamus of Macaca mulatta. Journal of Neurophysiology. 1989 Jan;61(1):114.Google Scholar
Ito, S, Craig, AD. Vagal-evoked activity in the parafascicular nucleus of the primate thalamus. Journal of Neurophysiology. 2005 Oct;94(4):29762982.Google Scholar
Evrard, HC, Craig, AD. Insular Cortex: Brain Mapping: Elsevier; 2015. pp. 387393.CrossRefGoogle Scholar
Craig, AD. Topographically organized projection to posterior insular cortex from the posterior portion of the ventral medial nucleus (VMpo) in the long-tailed macaque monkey. Journal of Comparative Neurology. 2014 Jul 13:36–63.Google Scholar
Hartig, R, Vedoveli, A, Logothetis, NK, Evrard, HC, editors. fMRI and electrophysiological mapping of sensory afferent activity in the macaque insular cortex. SfN Meeting; 2018; San Diego.Google Scholar
Baumgartner, U, Tiede, W, Treede, RD, Craig, AD. Laser-evoked potentials are graded and somatotopically organized anteroposteriorly in the operculoinsular cortex of anesthetized monkeys. Journal of Neurophysiology. 2006 Nov;96(5):28022808.CrossRefGoogle ScholarPubMed
Legrain, V, Iannetti, GD, Plaghki, L, Mouraux, A. The pain matrix reloaded: a salience detection system for the body. Prog Neurobiol. 2011 Jan;93(1):111124.CrossRefGoogle ScholarPubMed
Mazzola, L, Isnard, J, Peyron, R, Guenot, M, Mauguiere, F. Somatotopic organization of pain responses to direct electrical stimulation of the human insular cortex. Pain. 2009 Nov;146(1–2):99104.Google Scholar
Brooks, JC, Zambreanu, L, Godinez, A, Craig, AD, Tracey, I. Somatotopic organisation of the human insula to painful heat studied with high resolution functional imaging. NeuroImage. 2005 Aug 1;27(1):201209.Google Scholar
Hua, H, Strigo, IA, Baxter, LC, Johnson, SC, Craig, AD. Anteroposterior somatotopy of innocuous cooling activation focus in human dorsal posterior insular cortex. Am J Physiol Regul Integr Comp Physiol. 2005 Aug;289(2):R319R325.Google Scholar
Eickhoff, SB, Grefkes, C, Zilles, K, Fink, GR. The somatotopic organization of cytoarchitectonic areas on the human parietal operculum. Cerebral Cortex. 2007 Aug;17(8):18001811.Google Scholar
Wattendorf, E, Westermann, B, Lotze, M, Fiedler, K, Celio, MR. Insular cortex activity and the evocation of laughter. Journal of Comparative Neurology. 2016 Jun 1;524(8):16081615.Google Scholar
Bjornsdotter, M, Loken, L, Olausson, H, Vallbo, A, Wessberg, J. Somatotopic organization of gentle touch processing in the posterior insular cortex. Journal of Neuroscience. 2009 Jul 22;29(29):93149320.Google Scholar
Spetter, MS, de Graaf, C, Mars, M, Viergever, MA, Smeets, PA. The sum of its parts – effects of gastric distention, nutrient content and sensory stimulation on brain activation. PloS One. 2014;9(3):e90872.Google Scholar
Yaxley, S, Rolls, ET, Sienkiewicz, ZJ. Gustatory responses of single neurons in the insula of the macaque monkey. Journal of Neurophysiology. 1990 Apr;63(4):689700.Google Scholar
Ito, S, Ogawa, H. Neural activities in the fronto-opercular cortex of macaque monkeys during tasting and mastication. Jpn J Physiol. 1994;44(2):141156.Google Scholar
Small, DM. Taste representation in the human insula. Brain, Structure & Function. 2010 Jun;214(5–6):551561.Google Scholar
Wang, GJ, Tomasi, D, Backus, W, Wang, R, Telang, F, Geliebter, A, et al. Gastric distention activates satiety circuitry in the human brain. NeuroImage. 2008 Feb 15;39(4):18241831.Google Scholar
Avery, JA, Gotts, SJ, Kerr, KL, Burrows, K, Ingeholm, JE, Bodurka, J, et al. Convergent gustatory and viscerosensory processing in the human dorsal mid-insula. Human Brain Mapping. 2017 Apr;38(4):21502164.Google Scholar
Zhang, ZH, Dougherty, PM, Oppenheimer, SM. Characterization of baroreceptor-related neurons in the monkey insular cortex. Brain Research. 1998 Jun 15;796(1–2):303306.CrossRefGoogle ScholarPubMed
Zaki, J, Davis, JI, Ochsner, KN. Overlapping activity in anterior insula during interoception and emotional experience. NeuroImage. 2012 Aug 1;62(1):493499.Google Scholar
Bud Craig, AD. Central neural substrates involved in temperature discrimination, thermal pain, thermal comfort, and thermoregulatory behavior. Handbook of Clinical Neurology. 2018;156:317338.Google Scholar
Craig, AD, Chen, K, Bandy, D, Reiman, EM. Thermosensory activation of insular cortex. Nature Neuroscience. 2000 Feb;3(2):184190.Google Scholar
Brooks, JC, Nurmikko, TJ, Bimson, WE, Singh, KD, Roberts, N. fMRI of thermal pain: Effects of stimulus laterality and attention. NeuroImage. 2002 Feb;15(2):293301.Google Scholar
Drzezga, A, Darsow, U, Treede, RD, Siebner, H, Frisch, M, Munz, F, et al. Central activation by histamine-induced itch: analogies to pain processing: A correlational analysis of O-15 H2O positron emission tomography studies. Pain. 2001 May;92(1–2):295305.CrossRefGoogle ScholarPubMed
Olausson, H, Lamarre, Y, Backlund, H, Morin, C, Wallin, BG, Starck, G, et al. Unmyelinated tactile afferents signal touch and project to insular cortex. Nature Neuroscience. 2002 Sep;5(9):900904.Google Scholar
Hassanpour, MS, Simmons, WK, Feinstein, JS, Luo, Q, Lapidus, RC, Bodurka, J, et al. The insular cortex dynamically maps changes in cardiorespiratory interoception. Neuropsychopharmacology. 2018 Jan;43(2):426434.Google Scholar
Evrard, HC. Von Economo and fork neurons in the monkey insula, implications for evolution of cognition. Curr Op Behav Sci. 2018;21:182190.Google Scholar
Schneider, RJ, Friedman, DP, Mishkin, M. A modality-specific somatosensory area within the insula of the rhesus monkey. Brain Research. 1993 Sep 3;621(1):116120.Google Scholar
Jezzini, A, Rozzi, S, Borra, E, Gallese, V, Caruana, F, Gerbella, M. A shared neural network for emotional expression and perception: An anatomical study in the macaque monkey. Frontiers in Behavioral Neuroscience. 2015;9:243.Google Scholar
Stephani, C, Fernandez-Baca Vaca, G, Maciunas, R, Koubeissi, M, Luders, HO. Functional neuroanatomy of the insular lobe. Brain Structure & Function. 2011 Jun;216(2):137149.Google Scholar
Boucher, O, Rouleau, I, Lassonde, M, Lepore, F, Bouthillier, A, Nguyen, DK. Social information processing following resection of the insular cortex. Neuropsychologia. 2015 May;71:110.Google Scholar
Critchley, HD, Mathias, CJ, Dolan, RJ. Fear conditioning in humans: The influence of awareness and autonomic arousal on functional neuroanatomy. Neuron. 2002 Feb 14;33(4):653663.Google Scholar
Simmons, A, Strigo, I, Matthews, SC, Paulus, MP, Stein, MB. Anticipation of aversive visual stimuli is associated with increased insula activation in anxiety-prone subjects. Biological Psychiatry. 2006 Aug 15;60(4):402409.CrossRefGoogle ScholarPubMed
Borra, E, Gerbella, M, Rozzi, S, Luppino, G. The macaque lateral grasping network: A neural substrate for generating purposeful hand actions. Neuroscience and Biobehavioral Reviews. 2017 Apr;75:6590.Google Scholar
Remedios, R, Logothetis, NK, Kayser, C. An auditory region in the primate insular cortex responding preferentially to vocal communication sounds. Journal of Neuroscience. 2009 Jan 28;29(4):10341045.Google Scholar
Zhang, ZH, Dougherty, PM, Oppenheimer, SM. Monkey insular cortex neurons respond to baroreceptive and somatosensory convergent inputs. Neuroscience. 1999;94(2):351360.Google Scholar
Asahi, T, Uwano, T, Eifuku, S, Tamura, R, Endo, S, Ono, T, et al. Neuronal responses to a delayed-response delayed-reward go/nogo task in the monkey posterior insular cortex. Neuroscience. 2006 Dec 1;143(2):627639.CrossRefGoogle ScholarPubMed
Terasawa, Y, Fukushima, H, Umeda, S. How does interoceptive awareness interact with the subjective experience of emotion? An fMRI study. Human Brain Mapping. 2013 Mar;34(3):598612.CrossRefGoogle ScholarPubMed
Fuller, PM, Sherman, D, Pedersen, NP, Saper, CB, Lu, J. Reassessment of the structural basis of the ascending arousal system. Journal of Comparative Neurology 2011 Apr 1;519(5):933956.CrossRefGoogle ScholarPubMed
Parvizi, J, Damasio, AR. Neuroanatomical correlates of brainstem coma. Brain. 2003 Jul;126(pt 7):15241536.CrossRefGoogle ScholarPubMed
Sridharan, D, Levitin, DJ, Menon, V. A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proceedings of the National Academy of Sciences of the United States of America. 2008 Aug 26;105(34):1256912574.Google Scholar
Duncan, J. The multiple-demand (MD) system of the primate brain: Mental programs for intelligent behaviour. Trends in Cognitive Science. 2010 Apr;14(4):172179.Google Scholar
Wu, T, Wang, X, Wu, Q, Spagna, A, Yang, J, Yuan, C, et al. Anterior insular cortex is a bottleneck of cognitive control. NeuroImage. 2019 Feb 21:490504.Google Scholar
Wilk, HA, Ezekiel, F, Morton, JB. Brain regions associated with moment-to-moment adjustments in control and stable task-set maintenance. NeuroImage. 2012 Jan 16;59(2):19601967.Google Scholar
Warnaby, CE, Seretny, M, Ni Mhuircheartaigh, R, Rogers, R, Jbabdi, S, Sleigh, J, et al.Anesthesia-induced suppression of human dorsal anterior insula responsivity at loss of volitional behavioral response. Anesthesiol. 2016 Apr;124(4):766778.Google Scholar
Smith, R, Braden, BB, Chen, K, Ponce, FA, Lane, RD, Baxter, LC. The neural basis of attaining conscious awareness of sad mood. Brain Imaging and Behavior. 2015 Sep;9(3):574587.Google Scholar
Wang, L, Uhrig, L, Jarraya, B, Dehaene, S. Representation of numerical and sequential patterns in macaque and human brains. Current Biology. 2015 Aug 3;25(15):19661974.Google Scholar
Mitchell, DJ, Bell, AH, Buckley, MJ, Mitchell, AS, Sallet, J, Duncan, J. A putative multiple-demand system in the macaque. Brain. 2016 Aug 17;36(33):85748585.Google Scholar
Touroutoglou, A, Bliss-Moreau, E, Zhang, J, Mantini, D, Vanduffel, W, Dickerson, BC, et al. A ventral salience network in the macaque brain. NeuroImage. 2016 May 15;132:190197.Google Scholar
Critchley, H, Seth, A. Will studies of macaque insula reveal the neural mechanisms of self-awareness? Neuron. 2012 May 10;74(3):423426.CrossRefGoogle ScholarPubMed
Kaada, BR, Pribram, KH, Epstein, JA. Respiratory and vascular responses in monkeys from temporal pole, insula, orbital surface and cingulate gyrus: a preliminary report. Journal of Neurophysiology. 1949 Sep;12(5):347356.Google Scholar
Jezzini, A, Caruana, F, Stoianov, I, Gallese, V, Rizzolatti, G. Functional organization of the insula and inner peri-Sylvian regions. PNAS. 2012 Jun 19;109(25):1007710082.Google Scholar
Seth, AK, Friston, KJ. Active interoceptive inference and the emotional brain. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences. 2016 Nov 19;371(1708).Google Scholar
Michel, M. A role for the anterior insular cortex in the global neuronal workspace model of consciousness. Consciousness and Cognition. 2017 Mar;49:333346.Google Scholar
Fischer, DB, Boes, AD, Demertzi, A, Evrard, HC, Laureys, S, Edlow, BL, et al. A human brain network derived from coma-causing brainstem lesions. Neurology. 2016 Dec 6;87(23):24272434.CrossRefGoogle ScholarPubMed
Laureys, S, Boly, M, Moonen, G, Maquet, P. Two dimensions of consciousness: Arousal and awareness. Encycl Neurosci. 2009;2:11331142.Google Scholar
Azzalini, D, Rebollo, I, Tallon-Baudry, C. Visceral signals shape brain dynamics and cognition. Trends in Cognitive Sciences. 2019 Jun;23(6):488509.Google Scholar
Boly, M, Massimini, M, Tsuchiya, N, Postle, BR, Koch, C, Tononi, G. Are the neural correlates of consciousness in the front or in the back of the cerebral cortex? Clinical and neuroimaging evidence. Journal of Neuroscience. 2017 Oct 4;37(40):96039613.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×