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Right insula for our sense of limb ownership and self-awareness of actions

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Abstract

Normally, we are aware that our arms and legs belong to us and not to someone else. However, some stroke patients with hemiparesis/-plegia after right-sided stroke show a disturbed sensation of limb ownership and a disturbed self-awareness of actions and such patients with anosognosia for hemiparesis/plegia typically deny their paresis/-plegia and are convinced that their limbs function normally. They may experience their limb(s) as not belonging to them and may even attribute them to other persons. Modern lesion analyses techniques in such patients and recent neuroimaging results in healthy subjects suggest a prominent role of the right insula for our sense of limb ownership as well as for our feeling of being involved in a movement—our sense of agency. We thus hypothesize that the right insular cortex constitutes a central node of a network involved in human body scheme representation.

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References

  • André JM, Martinet N, Paysant J, Beis JM, Le Chapelain L (2001) Temporary phantom limbs evoked by vestibular caloric stimulation in amputees. Neuropsychiatry Neuropsychol Behav Neurol 14:190–196

    PubMed  Google Scholar 

  • Appelros P, Karlsson GM, Seiger A, Nydevik I (2002) Neglect and anosognosia after firstever stroke: incidence and relationship to disability. J Rehabil Med 34:215–220

    Article  PubMed  Google Scholar 

  • Augustine JR (1996) Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Rev 22:229–244

    Article  CAS  PubMed  Google Scholar 

  • Baier B, Karnath HO (2005) Incidence and diagnosis of anosognosia for hemiparesis. J Neurol Neurosurg Psychiatry 76:358–361

    Article  CAS  PubMed  Google Scholar 

  • Baier B, Karnath HO (2008) Tight link between our sense of limb ownership and self-awareness of actions. Stroke 39:486–488

    Article  PubMed  Google Scholar 

  • Baier B, Bense S, Birklein F, Buchholz HG, Mischke A, Schreckenberger M, Dieterich M (2010) Evidence for modulation of opioidergic activity in central vestibular processing: A [18F] diprenorphine PET study. Hum Brain Mapp 31:550–555

    PubMed  Google Scholar 

  • Bense S, Bartenstein P, Lochmann M, Schlindwein P, Brandt T, Dieterich M (2004) Metabolic changes in vestibular and visual cortices in acute vestibular neuritis. Ann Neurol 56:624–630

    Article  PubMed  Google Scholar 

  • Berti A, Bottini G, Gandola M, Pia L, Smania N, Stracciari A, Castiglioni I, Vallar G, Paulesu E (2005) Shared cortical anatomy for motor awareness and motor control. Science 309:488–491

    Article  CAS  PubMed  Google Scholar 

  • Bisiach E, Rusconi ML, Vallar G (1991) Remission of somatoparaphrenic delusion through vestibular stimulation. Neuropsychologia 29:1029–1031

    Article  CAS  PubMed  Google Scholar 

  • Blanke O, Landis T, Spinelli L, Seeck M (2004) Out-of-body experience and autoscopy of neurological origin. Brain 127:243–258

    Article  PubMed  Google Scholar 

  • Bottini G, Sterzi R, Paulesu E, Vallar G, Cappa SF, Erminio F, Passingham RE, Frith CD, Frackowiak RS (1994) Identification of the central vestibular projections in man: a positron emission tomography activation study. Exp Brain Res 99:164–169

    Article  CAS  PubMed  Google Scholar 

  • Bottini G, Karnath HO, Vallar G, Sterzi R, Frith CD, Frackowiak RS, Paulesu E (2001) Cerebral representations for egocentric space: functional-anatomical evidence from caloric vestibular stimulation and neck vibration. Brain 124:1182–1196

    Article  CAS  PubMed  Google Scholar 

  • Botvinick M (2004) Probing the neural basis of body ownership. Science 305:782–783

    Article  CAS  PubMed  Google Scholar 

  • Botvinick M, Cohen J (1998) Rubber hands “feel” touch that eyes see. Nature 391:756

    Article  CAS  PubMed  Google Scholar 

  • Brandt T, Dieterich M, Danek A (1994) Vestibular cortex lesions affect the perception of verticality. Ann Neurol 35:403–412

    Article  CAS  PubMed  Google Scholar 

  • Breier Jl, Adair JC, Gold M, Fennell EB, Gilmore RL, Heilman KM (1995) Dissociation of anosognosia for hemiplegia and aphasia during left-hemisphere anesthesia. Neurology 45:65–67

    CAS  PubMed  Google Scholar 

  • Brooks JC, Nurmikko TJ, Bimson WE, Singh KD, Roberts N (2002) fMRI of thermal pain: effects of stimulus laterality and attention. Neuroimage 15:293–301

    Article  PubMed  Google Scholar 

  • Cappa S, Sterzi R, Vallar G, Bisiach E (1987) Remission of hemineglect and anosognosia during vestibular stimulation. Neuropsychologia 25:775–783

    Article  CAS  PubMed  Google Scholar 

  • Cereda C, Ghika J, Maeder P, Bogousslavsky J (2002) Strokes restricted to the insular cortex. Neurology 59:1950–1955

    CAS  PubMed  Google Scholar 

  • Cocchini G, Beschin N, Cameron A, Fotopoulou A, Della Sala S (2009) Anosognosia for motor impairment following left brain damage. Neuropsychology 23:223–230

    Article  PubMed  Google Scholar 

  • Contreras M, Ceric F, Torrealba F (2007) Inactivation of the interoceptive insula disrupts drug craving and malaise induced by lithium. Science 318:655–658

    Article  CAS  PubMed  Google Scholar 

  • Corradi-Dell’ Acqua C, Ueno K, Ogawa A, Cheng K, Rumiata RI, Iriki A (2008) Effects of shifting perspective of the self: an fMRI study. Neuroimage 40:1902–1911

    Article  Google Scholar 

  • Craig AD (2002) How do you feel? Interoception: the sense of physiological condition of the body. Nat Rev Neurosci 3:655–666

    CAS  PubMed  Google Scholar 

  • Craig AD (2009) How do you feel-now? The anterior insula and human awareness. Nat Rev Neurosci 10:59–70

    Article  CAS  PubMed  Google Scholar 

  • Craig AD (2010) The insular cortex and subjective feeling states. In: Prigatano GP (ed) The study of anosognosia. Oxford University Press, Oxford

  • Craig AD, Reiman EM, Evans A, MCl Bushnell (1996) Functional imaging of an illusion of pain. Nature 384:258–260

    Article  CAS  PubMed  Google Scholar 

  • Craig AD, Chen K, Bandy D, Reiman EM (2000) Thermosensory activation of insular cortex. Nat Neurosci 3:184–190

    Article  CAS  PubMed  Google Scholar 

  • Cutting J (1978) Study of anosognosia. J Neurol Neurosurg Psychiatry 41:548–555

    Article  CAS  PubMed  Google Scholar 

  • Damasio AR, Grabowski TJ, Bechara A, Damasio H, Ponto LLB, Parvizi J, Hichwa RD (2000) Subcortical and cortical brain activity during the feeling of self-generated emotions. Nat Neurosci 3:1049–1056

    Article  CAS  PubMed  Google Scholar 

  • Devue C, Collette F, Balteau E, Degueldre C, Luxen A, Maquet P, Brédart S (2007) Here I am: the cortical correlates of visual self-recognition. Brain Res 1143:169–182

    Article  CAS  PubMed  Google Scholar 

  • Dieterich M, Brandt T (2008) Functional brain imaging of peripheral and central vestibular disorders. Brain 131:2538–2552

    Article  PubMed  Google Scholar 

  • Dronkers NF (1996) A new brain region for coordinating speech articulation. Nature 384:159–161

    Article  CAS  PubMed  Google Scholar 

  • Ehrsson HH, Wiech K, Weiskopf N, Dolan RJ, Passingham RE (2007) Threatening a rubber hand that you feel is yours elicits a cortical anxiety response. Proc Natl Acad Sci USA 104:9828–9833

    Article  CAS  PubMed  Google Scholar 

  • Eickhoff SB, Weiss PH, Amunts K, Fink GR, Zilles K (2006) Identifying human parieto-insular vestibular cortex using fMRI and cytoarchitectonic mapping. Hum Brain Mapp 27:611–621

    Article  PubMed  Google Scholar 

  • Emri M, Kisely M, Lengyel Z, Balkay L, Márián T, Mikó L, Berényi E, Sziklai I, Trón L, Tóth A (2003) Cortical projection of peripheral vestibular signaling. J Neurophysiol 89:2639–2646

    Article  PubMed  Google Scholar 

  • Farrell MJ, Egan GF, Zamarripa F, Shade R, Blair-West J, Fox P, Denton DA (2006) Unique, common, and interacting cortical correlates of thirst and pain. Proc Natl Acad Sci USA 103:2416–2421

    Article  CAS  PubMed  Google Scholar 

  • Farrer C, Franck N, Georgieff N, Frith CD, Decety J, Jeannerod M (2003) Modulating the experience of agency: a positron emission tomography study. Neuroimage 18:324–333

    Article  CAS  PubMed  Google Scholar 

  • Farrer C, Franck N, Frith CD, Decety J, Georgieff N, d’Amato T, Jeannerod M (2004) Neural correlates of action attribution in schizophrenia. Psychiatry Res 131:31–44

    Article  PubMed  Google Scholar 

  • Farrer C, Frey SH, Van Horn JD, Tunik E, Turk D, Inati S, Grafton ST (2008) The angular gyrus computes action awareness representations. Cereb Cortex 18:254–261

    Article  PubMed  Google Scholar 

  • Faurion A, Cerf B, Le Bihan D, Pillias A-M (1998) fMRI study of taste cortical areas in humans. Ann N Y Acad Sci 855:535–545

    Article  CAS  PubMed  Google Scholar 

  • Felician O, Anton JL, Nazarian B, Roth M, Roll JP, Romaiguère P (2009) Where is your shoulder? Neural correlates of localizing others’ body parts. Neuropsychologia 47:1909–1916

    Article  PubMed  Google Scholar 

  • Fiol ME, Leppick IE, Mireles R, Maxwell R (1988) Ictus emeticus and the insular cortex. Epilepsy Res 2:127–131

    Article  CAS  PubMed  Google Scholar 

  • Frot M, Mauguière F (2003) Dual representation of pain in the operculo-insular cortex in humans. Brain 126:438–450

    Article  PubMed  Google Scholar 

  • Gilmore RL, Heilman KM, Schmidt RP, Fennell EM, Quisling R (1992) Anosognosia during Wada testing. Neurology 42:925–927

    CAS  PubMed  Google Scholar 

  • Griffiths D, Tadic SD, Schaefer W, Resnick NM (2007) Cerebral control of the bladder in normal and urge-incontinent women. Neuroimage 37:1–7

    Article  PubMed  Google Scholar 

  • Humbert IA, Robbins J (2007) Normal swallowing and functional magnetic resonance imaging: a systematic review. Dysphagia 22:266–275

    Article  PubMed  Google Scholar 

  • Karnath HO (2009) A right perisylvian neural network for human spatial orienting. In: Gazzaniga MS (ed) The cognitive neurosciences IV. MIT Press, Cambridge, pp 259–268

    Google Scholar 

  • Karnath HO, Baier B (2010) Anosognosia for hemiparesis and hemiplegia: disturbed sense of agency and body ownership. In: Prigatano GP (ed) The study of anosognosia. Oxford University Press, Oxford

  • Karnath HO, Ferber S, Himmelbach M (2001) Spatial awareness is a function of the temporal not the posterior parietal lobe. Nature 411:950–953

    Article  CAS  PubMed  Google Scholar 

  • Karnath HO, Fruhmann Berger M, Küker W, Rorden C (2004) The anatomy of spatial neglect based on voxelwise statistical analysis: a study of 140 patients. Cereb Cortex 14:1164–1172

    Article  PubMed  Google Scholar 

  • Karnath HO, Baier B, Nägele T (2005) Awareness of the functioning of one’s own limbs mediated by the insular cortex? J Neurosci 25:7134–7138

    Article  CAS  PubMed  Google Scholar 

  • Kimmerly DS, O’Leary DD, Menon RS, Gati JS, Shoemaker JK (2005) Cortical regions associated with autonomic cardiovascular regulation during lower body negative pressure in humans. J Physiol 569:331–345

    Article  CAS  PubMed  Google Scholar 

  • Kong J, White NS, Kwong KK, Vangel MG, Rosman IS, Gracely RH, Gollub RL (2006) Using fMRI to dissociate sensory encoding from cognitive evaluation of heat pain intensity. Hum Brain Mapp 27:715–721

    Article  PubMed  Google Scholar 

  • Lopez C, Halje P, Blanke O (2008) Body ownership and embodiment: vestibular and multisensory mechanisms. Neurophysiol Clin 38:149–161

    Article  CAS  PubMed  Google Scholar 

  • Maihöfner C, Kaltenhäuser M, Neundörfer B, Lang E (2002) Temporo-spatial analysis of cortical activation by phasic innocuous and noxious cold stimuli—a magnetoencephalographic study. Pain 100:281–290

    Article  PubMed  Google Scholar 

  • Mesulam MM, Mufson EJ (1985) The insula of reil in man and monkey. Architectonics, connectivity, and function. In: Peters A, Jones EG (eds) Cerebral cortex. Plenum Press, New York, pp 179–226

    Google Scholar 

  • Moseley GL, Olthof N, Venema A, Don S, Wijers M, Gallace A, Spence C (2008) Psychologically induced cooling of a specific body part caused by the illusory ownership of an artificial counterpart. Proc Natl Acad Sci USA 105:13169–13173

    Article  CAS  PubMed  Google Scholar 

  • Naqvi NH, Rudrauf D, Damasio H, Bechara A (2007) Damage to the insula disrupts addiction to cigarette smoking. Science 315:531–534

    Article  CAS  PubMed  Google Scholar 

  • Nathanson M, Bergman P, Gordon G (1952) Denial of illness. Its occurrence in one hundred consecutive cases of hemiplegia. Arch Neurol Psychiatry 68:380–387

    CAS  Google Scholar 

  • Ogawa H, Wakita M, Hasegawa K, Kobayakawa T, Sakai N, Hirai T, Yamashita Y, Saito S (2005) Functional MRI detection of activation in the primary gustatory cortices in humans. Chem Senses 30:583–592

    Article  CAS  PubMed  Google Scholar 

  • Paulus MP, Stein MB (2006) An insular view of anxiety. Biol Psychiatry 60:383–387

    Article  PubMed  Google Scholar 

  • Phillips ML, Young AW, Senior C, Brammer M, Andrew C, Calder AJ, Bullmore ET, Perrett DI, Rowland D, Williams SCR, Gray JA, David AS (1997) A specific neural substrate for perceiving facial expressions of disgust. Nature 389:495–498

    Article  CAS  PubMed  Google Scholar 

  • Rode G, Charles N, Perenin MT, Vighetto A, Trillet M, Aimard G (1992) Partial remission of hemiplegia and somatoparaphrenia through vestibular stimulation in a case of unilateral neglect. Cortex 28:203–208

    CAS  PubMed  Google Scholar 

  • Rorden C, Karnath HO (2004) Using human brain lesions to infer function: a relic from a past era in the fMRI age? Nat Rev Neurosci 5:813–819

    Article  PubMed  Google Scholar 

  • Rorden C, Karnath HO, Bonilha L (2007) Improving lesion-symptom mapping. J Cogn Neurosci 19:1081–1088

    Article  PubMed  Google Scholar 

  • Rorden C, Fridriksson J, Karnath HO (2009) An evaluation of traditional and novel tools for lesion behavior mapping. Neuroimage 44:1355–1362

    Article  PubMed  Google Scholar 

  • Sang FY, Jáuregui-Renaud K, Green DA, Bronstein AM, Gresty MA (2006) Depersonalisation/derealisation symptoms in vestibular disease. J Neurol Neurosurg Psychiatry 77:760–766

    Article  PubMed  Google Scholar 

  • Schneider RC, Calhoun HD, Kooi KA (1971) Circling and rotational automatisms in patients with frontotemporal cortical and subcortical lesions. J Neurosurg 35:554–563

    Article  CAS  PubMed  Google Scholar 

  • Schneider RJ, Friedman DP, Mishkin M (1993) A modality-specific somatosensory area within the insula of the rhesus monkey. Brain Res 621:116–120

    Article  CAS  PubMed  Google Scholar 

  • Schreckenberger M, Siessmeier T, Viertmann A, Landvogt C, Buchholz HG, Rolke R, Treede RD, Bartenstein P, Birklein F (2005) The unpleasantness of tonic pain is encoded by the insular cortex. Neurology 64:1175–1183

    CAS  PubMed  Google Scholar 

  • Showers MJC, Laucer EW (1961) Somatovisceral motor patterns in the insula. J Comp Neurol 117:107–115

    Article  CAS  PubMed  Google Scholar 

  • Starkstein SE, Fedoroff JP, Price TR, Leiguarda R, Robinson RG (1992) Anosognosia in patients with cerebrovascular lesions. Stroke 23:1446–1453

    CAS  PubMed  Google Scholar 

  • Stein MB, Simmons AN, Feinstein JS, Paulus MP (2007) Increased amygdala and insula activation during emotion processing in anxiety-prone subjects. Am J Psychiatry 164:318–327

    Article  PubMed  Google Scholar 

  • Sugar O, Chusid JG, French JD (1948) A second motor cortex in the monkey (Macaca mulatta). J Neuropathol Exp Neurol 7:182–189

    Article  CAS  PubMed  Google Scholar 

  • Tsakiris A, Hesse MD, Boy C, Haggard P, Fink GR (2007) Neural signatures of body ownership: a sensory network for bodily self-consciousness. Cereb Cortex 17:2235–2244

    Article  PubMed  Google Scholar 

  • Vocat R, Vuilleumier P (2010) Neuroanatomy of impaired body awareness in anosognosia and hysteria: a multi-component account. In: Prigatano GP (ed) The study of anosognosia. Oxford University Press, Oxford

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Acknowledgments

This work was supported by the Bundesministerium für Bildung und Forschung (BMBF-Verbundprojekt “Räumliche Orientierung” 01GW0641) and the Deutsche Forschungsgemeinschaft (KA 1258/10-1).

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  1. Section of Neuropsychology, Center of Neurology, Hertie-Institute for Clinical Brain Research, University of Tübingen, Hoppe-Seyler-Str. 3, 72076, Tübingen, Germany

    Hans-Otto Karnath

  2. Department of Neurology, University of Mainz, Mainz, Germany

    Bernhard Baier

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  1. Hans-Otto Karnath
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Correspondence to Hans-Otto Karnath.

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Karnath, HO., Baier, B. Right insula for our sense of limb ownership and self-awareness of actions. Brain Struct Funct 214, 411–417 (2010). https://doi.org/10.1007/s00429-010-0250-4

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