Top

Published in:

01-06-2010 | Original article

The insular cortex: a comparative perspective

Authors: Camilla Butti, Patrick R. Hof

Published in: Brain Structure and Function | Issue 5-6/2010

Abstract

The human insular cortex is involved in a variety of viscerosensory, visceromotor, and interoceptive functions, and plays a role in complex processes such as emotions, music, and language. Across mammals, the insula has considerable morphologic variability. We review the structure and connectivity of the insula in laboratory animals (mouse, domestic cat, macaque monkey), and we present original data on the morphology and cytoarchitecture of insular cortex in less common species including a large carnivore (the Atlantic walrus, Odobenus rosmarus), two artiodactyls (the pigmy hippopotamus, Hexaprotodon liberiensis, and the Western bongo, Tragelaphus eurycerus), two cetaceans (the beluga whale, Delphinapterus leucas, and the minke whale, Balaenoptera acutorostrata), and a sirenian (the Florida manatee, Trichechus manatus latirostris). The insula shows substantial variability in shape, extent, and gyral and sulcal patterns, as well as differences in laminar organization, cellular specialization, and structural association with the claustrum. Our observations reveal that the insular cortex is extremely variable among mammals. These differences could be related to the role exerted by specific and selective pressures on cortical structure during evolution. We conclude that it is not possible to identify a general model of organization for the mammalian insular cortex.

Ackermann H, Riecker A (2010) The contribution(s) of the insula to speech communication: a review of the clinical and functional imaging literature. Brain Struct Funct 214(5–6). doi:10.1007/s00429-010-0257-x (this issue)

Aggleton JP, Burton MJ, Passingham RE (1980) Cortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca mulatta). Brain Res 190:347–368CrossRefPubMed

Agnarsson I, May-Collado LJ (2008) The phylogeny of Cetartiodactyla: the importance of dense taxon sampling, missing data, and the remarkable promise of cytochrome b to provide reliable species-level phylogenies. Mol Phylogenet Evol 48:964–985CrossRefPubMed

Aleksandrov VG, Fedorova KP (2003) Structure of the insular region of the rat neocortex. Neurosci Behav Physiol 33:199–202CrossRefPubMed

Allman JM, Tetreault NA, Hakeem AY, Manaye KF, Semendeferi K, Erwin JM, Goubert V, Hof PR (2010) The von Economo neurons in frontoinsular and anterior cingulate cortex of great apes and humans. Brain Struct Funct 214(5–6). doi:10.1007/s00429-010-0254-0 (this issue)

Augustine JR (1985) The insular lobe in primates including humans. Neurol Res 7:2–10PubMed

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

Bamiou DE, Musiek FE, Luxon LM (2003) The insula (island of Reil) and its role in auditory processing. Literature review. Brain Res 42:143–154CrossRef

Barklow WE (1997) Some underwater sounds of the hippopotamus (Hippopotamus amphibius). Mar Freshw Behav Physiol 29:237–249CrossRef

Barklow WE (2004) Amphibious communication with sound in hippos, Hippopotamus amphibius. Anim Behav 68:1125–1132CrossRef

Boisserie JR, Lihoreau F, Brunet M (2005) The position of Hippopotamidae within Cetartiodactyla. Proc Natl Acad Sci USA 102:1537–1541CrossRefPubMed

Burton H, Videen TO, Raichle ME (1993) Tactile-vibration-activated foci in insular and parietal-opercular cortex studied with positron emission tomography: mapping the second somatosensory area in humans. Somat Mot Res 10:297–308CrossRef

Butti C, Sherwood CC, Hakeem AY, Allman JM, Hof PR (2009) Total number and volume of von Economo neurons in the cerebral cortex of cetaceans. J Comp Neurol 515:243–259CrossRefPubMed

Chikama M, McFarland NR, Amaral DG, Haber SN (1997) Insular cortical projections to functional regions of the striatum correlate with cortical cytoarchitectonic organization in the primate. J Neurosci 17:9686–9705PubMed

Clasca F, Llamas A, Reinoso-Suarez F (1997) Insular cortex and neighboring fields in the cat: a redefinition based on cortical microarchitecture and connections with the thalamus. J Comp Neurol 384:456–482CrossRefPubMed

Clemens ET, Malioy GMO (1982) The digestive physiology of three East African herbivores: the elephant, rhinoceros and hippopotamus. J Zool 198:141–156CrossRef

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

Craig AD (2003) Interoception: the sense of the physiological condition of the body. Curr Opin Neurobiol 13:500–505CrossRefPubMed

Craig AD (2009a) Emotional moments across time: a possible neural basis for time perception in the anterior insula. Philos Trans R Soc Lond 364:1933–1942CrossRef

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

Craig AD (2010) The sentient self. Brain Struct Funct 214(5–6). doi:10.1007/s00429-010-0248-y (this issue)

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

Critchley HD (2005) Neural mechanisms of autonomic, affective, and cognitive integration. J Comp Neurol 493:154–166CrossRefPubMed

Critchley HD, Wiens S, Rotshtein P, Ohman A, Dolan RJ (2004) Neural systems supporting interoceptive awareness. Nat Neurosci 7:189–195CrossRefPubMed

De Jong WW, Zweers A, Goodman M (1981) Relationship of aardvark to elephants, hyraxes, and sea cows from α-crystallin sequences. Nature 292:538–540CrossRefPubMed

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

Dexler H (1913) Das Hirn von Halicore Dugong. Erxl Gegenbaurs Morphol Jahrb 45:97–190

Eltringham SK (1993) The pygmy hippopotamus (Hexaprotodon liberiensis). In: Oliver WLR (ed) Pigs, peccaries and hippos: status survey and action plan. IUCN, Gland, Switzerland, pp 87–94

Eltringham SK (1999) The hippos. Academic Press, London

Fajardo C, Escobar MI, Buritica E, Arteaga G, Umbarila J, Casanova MF, Pimienta H (2008) Von Economo neurons are present in the dorsolateral (dysgranular) prefrontal cortex of humans. Neurosci Lett 435:215–218CrossRefPubMed

Friedman DP, Murray EA, O’Neill JB, Mishkin M (1986) Cortical connections of the somatosensory fields of the lateral sulcus of macaques: evidence for a corticolimbic pathway for touch. J Comp Neurol 252:323–347CrossRefPubMed

Gatesy J (1997) More DNA support for a Cetacea/Hippopotamidae clade: the blood-clotting protein gene gamma-fibrinogen. Mol Biol Evol 14:537–543PubMed

Gedamke J, Costa DP, Dunstan A (2001) Localization and visual verification of a complex minke whale vocalization. J Acoust Soc Am 109:3038–3047CrossRefPubMed

Getty R (1975) Digestive system. In: Sisson S, Grossman R (eds) The anatomy of the domestic animals, vol 1. WB Saunders, Philadelphia, PA, pp 470–497

Gray RW (1927) The walrus. Nature 119:923CrossRef

Gu X, Liu X, Guise KG, Naidich TP, Hof PR, Fan J (2010) Functional dissociation of the frontoinsular and anterior cingulate cortices in empathy for pain. J Neurosci 30:3739–3744CrossRefPubMed

Hakeem AY, Sherwood CC, Bonar CJ, Butti C, Hof PR, Allman JM (2009) Von Economo neurons in the elephant brain. Anat Rec 292:242–248CrossRef

Hassiotis M, Paxinos G, Ashwell KWS (2004) Cyto- and chemoarchitecture of the cerebral cortex of the Australian echidna (Tachyglossus aculeatus). I. Areal organization. J Comp Neurol 475:493–517CrossRefPubMed

Hof PR, Van der Gucht E (2007) Structure of the cerebral cortex of the humpback whale, Megaptera novaeangliae (Cetacea, Mysticeti, Balaenopteridae). Anat Rec 290:1–31CrossRef

Hof PR, Young WG, Bloom FE, Belichenko PV, Celio MR (2000) Comparative cytoarchitectonic atlas of the C57BL/6 and 129/Sv mouse brains. Elsevier, Amsterdam

Hof PR, Chanis R, Marino L (2005) Cortical complexity in cetacean brains. Anat Rec 287:1142–1152CrossRef

Hoffman BL, Rasmussen T (1953) Stimulation studies of insular cortex of Macaca mulatta. J Neurophysiol 16:343–351PubMed

Höistad M, Barbas H (2008) Sequence of information processing for emotions through pathways linking temporal and insular cortices with the amygdala. NeuroImage 40:1016–1033CrossRefPubMed

Hungate RE, Phillips GD, McGregor A, Hungate DP, Buechner HK (1959) Microbial fermentation in certain mammals. Science 130:1192–1194CrossRefPubMed

Insausti R, Amaral DG, Cowan WM (1987) The entorhinal cortex of the monkey: II. Cortical afferents. J Comp Neurol 264:356–395CrossRefPubMed

Jacobs MS, Morgane PJ, McFarland WL (1971) The anatomy of the brain of the bottlenose dolphin (Tursiops truncatus). Rhinic lobe (rhinencephalon). I. The paleocortex. J Comp Neurol 141:205–271CrossRefPubMed

Jacobs MS, McFarland WL, Morgane PJ (1979) The anatomy of the brain of the bottlenose dolphin (Tursiops truncatus). Rhinic lobe (Rhinencephalon): the archicortex. Brain Res Bull 4(Suppl 1):1–108CrossRefPubMed

Jacobs MS, Galaburda AM, McFarland WL, Morgane PJ (1984) The insular formations of the dolphin brain: quantitative cytoarchitectonic studies of the insular component of the limbic lobe. J Comp Neurol 225:396–432CrossRefPubMed

Johnson JI, Buchanan KJ, Morris JA, Fobbs AJ Jr (2009) Interrelation of gyral formation, cytoarchitectural variations, and sensory regions in human insular cortex. Program No 464.9/DD1, 2009 Neuroscience Meeting Planner. Society for Neuroscience, Chicago, IL (Online)

Jürgens U (1982) Afferents to the cortical larynx area in the monkey. Brain Res 239:377–389CrossRefPubMed

Karnath HO, Baier B (2010) Right insula for our sense of limb ownership and self-awareness of actions. Brain Struct Funct 214(5–6). doi:10.1007/s00429-010-0250-4 (this issue)

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

Kastelein RA (2008) Walrus (Odobenus rosmarus). In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of marine mammals. Academic Press, San Diego, CA, pp 1212–1217

Kingdon J (1982) East African mammals vol IIIC. The University of Chicago Press, Chicago

Kosillo P, Smith AT (2010) The role of the human anterior insular cortex in time processing. Brain Struct Funct 214(5–6) (this issue)

Lamm C, Singer T (2010) The role of anterior insular cortex in social emotions. Brain Struct Funct 214(5–6). doi:10.1007/s00429-010-0251-3 (this issue)

Langworthy O (1932) A description of the central nervous system of the porpoise (Tursiops truncatus). J Comp Neurol 350:337–356

Manger P, Sum M, Szymanski M, Ridgway SH, Krubitzer L (1998) Modular subdivisions of dolphin insular cortex: does evolutionary history repeat itself? J Cogn Neurosci 10:153–166CrossRefPubMed

Marino L (1998) A comparison of encephalization between Odontocete cetaceans and Anthropoid primates. Brain Behav Evol 51:230–238CrossRefPubMed

Marino L (2008) Brain size evolution. In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of marine mammals. Academic Press, San Diego, CA, pp 149–152

Marino L, McShea D, Uhen MD (2004) The origin and evolution of large brains in toothed whales. Anat Rec 281A:1247–1255CrossRef

Marino L, Connor RC, Fordyce RE, Herman LM, Hof PR, Lefebvre L, Lusseau D, McCowan B, Nimchinsky EA, Pack AA, Rendell L, Reidenberg JS, Reiss D, Uhen MD, Van der Gucht E, Whitehead H (2007) Cetaceans have complex brains for complex cognition. PLoS Biol 5(5):e139CrossRefPubMed

Marshall CD, Reep RL (1995) Manatee cerebral cortex: cytoarchitecture of the caudal region in Trichechus manatus latirostris. Brain Behav Evol 45:1–18CrossRefPubMed

Mesulam MM, Mufson EJ (1982a) Insula of the old world monkey. I. Architectonics in the insulo-orbito-temporal component of the paralimbic brain. J Comp Neurol 212:1–22CrossRefPubMed

Mesulam MM, Mufson EJ (1982b) Insula of the old world monkey. III: efferent cortical output and comments on function. J Comp Neurol 212:38–52CrossRefPubMed

Mesulam MM, Mufson EJ (1985) The insula of Reil in man and monkey. Architectonics, connectivity and function. In: Jones EG, Peters A (eds) Cerebral cortex, vol 4. Plenum Press, New York, pp 179–226

Morgane PJ, Jacobs MS, McFarland WL (1980) The anatomy of the brain of the bottlenose dolphin (Tursiops truncatus). Surface configuration of the telencephalon of the bottlenose dolphin with comparative anatomical observations in four other cetaceans species. Brain Res Bull 5:1–107CrossRef

Morgane PJ, McFarland WL, Jacobs MS (1982) The limbic lobe of the dolphin brain: a quantitative cytoarchitectonic study. J Hirnforsch 23:465–552PubMed

Mufson EJ, Mesulam MM (1982) Insula of the old world monkey. II: afferent cortical input and comments on the claustrum. J Comp Neurol 212:23–37CrossRefPubMed

Mufson EJ, Mesulam MM, Pandya DN (1981) Insular interconnections with the amygdala in the rhesus monkey. Neuroscience 6:1231–1248CrossRefPubMed

Murphy WJ, Eizirik E, O’Brien SJ, Madsen O, Scally M, Douady CJ, Teeling E, Ryder OA, Stanhope MJ, de Jong WW, Springer MS (2001) Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294:2348–2351CrossRefPubMed

Mutschler I, Schulze-Bonhage A, Glauche V, Demandt E, Speck O, Ball T (2007) A rapid sound-action association effect in human insular cortex. PLoS One 2(2):e259CrossRefPubMed

Mutschler I, Wieckhorst B, Kowalevski S, Derix J, Wentlandt J, Schulze-Bonhage A, Ball T (2009) Functional organization of the human anterior insular cortex. Neurosci Lett 457:66–70CrossRefPubMed

Naqvi NH, Bechara A (2010) The insula and drug addiction: an interoceptive view of pleasure, urges and decision-making. Brain Struct Funct 214(5–6). doi:10.1007/s00429-010-0268-7 (this issue)

Nimchinsky EA, Vogt BA, Morrison JH, Hof PR (1995) Spindle neurons of the human anterior cingulate cortex. J Comp Neurol 355:27–37CrossRefPubMed

Nimchinsky EA, Gilissen E, Allman JM, Perl DP, Erwin JM, Hof PR (1999) A neuronal morphologic type unique to humans and great apes. Proc Natl Acad Sci USA 96:5268–5273CrossRefPubMed

O’Corry-Crowe GM (2008) Beluga whale (Delphinapterus leucas). In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of marine mammals. Academic Press, San Diego, CA, pp 108–112

Oelschläger HHA, Oelschläger J (2008) Brain. In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of marine mammals. Academic Press, San Diego, CA, pp 134–149

Pandya DN, Van Hoesen GW, Mesulam MM (1981) Efferent connections of the cingulate gyrus in the rhesus monkey. Exp Brain Res 42:319–330CrossRefPubMed

Paulus MP, Stein MB (2010) Interoception in anxiety and depression. Brain Struct Funct 214(5–6). doi:10.1007/s00429-010-0258-9 (this issue)

Penfield W, Faulk ME Jr (1955) The insula; further observations on its function. Brain 78:445–470CrossRefPubMed

Perrin WF, Brownell RL Jr (2008) Minke whales (Balaenoptera acutorostrata and B. bonaerensis). In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of marine mammals. Academic Press, San Diego, CA, pp 733–735

Platel H, Price C, Baron JC, Wise R, Lambert J, Frackowiak RS, Lechevalier B, Eustache F (1997) The structural components of music perception. A functional anatomical study. Brain 120:229–243CrossRefPubMed

Pritchard TC, Hamilton RB, Morse JR, Norgren R (1986) Projections of thalamic gustatory and lingual areas in the monkey, Macaca fascicularis. J Comp Neurol 244:213–228CrossRefPubMed

Pritchard TC, Macaluso DA, Eslinger PJ (1999) Taste perception in patients with insular cortex lesions. Behav Neurosci 113:663–671CrossRefPubMed

Reep RL, O’Shea TJ (1990) Regional brain morphometry and lissencephaly in the Sirenia. Brain Behav Evol 35:185–194CrossRefPubMed

Reep RL, Johnson JI, Switzer RC, Welker WI (1989) Manatee cerebral cortex: cytoarchitecture of the frontal region in Trichechus manatus latirostris. Brain Behav Evol 34:365–386CrossRefPubMed

Revishchin AV, Garey LJ (1990) The thalamic projection to the sensory neocortex of the porpoise, Phocoena phocoena. J Anat 169:85–102PubMed

Reynolds JE III, Rommel SA (1996) Structure and function of the gastrointestinal tract of the Florida manatee, Trichechus manatus latirostris. Anat Rec 245:539–558CrossRefPubMed

Reynolds JE III, Rommel SA (2008) Anatomical dissection: thorax and abdomen. In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of marine mammals. Academic Press, San Diego, CA, pp 29–36

Reynolds JE III, Powell JA, Taylor CR (2008) Manatees (Trichechus manatus, T. senegalensis, and T. inunguis). In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of marine mammals. Academic Press, San Diego, CA, pp 682–691

Ries E, Langworthy O (1937) A study of the surface structure of the brain of the whale (Balaenoptera physalus and Physeter catodon). J Comp Neurol 68:1–47CrossRef

Rose M (1928) Die Inselrinde des Menschen und der Tiere. J Psychol Neurol 37:467–624

Rose JE (1942) A cytoarchitectural study of the sheep cortex. J Comp Neurol 76:1–55CrossRef

Russo D, Paparcone R, Genovese A (2008) A cytoarchitectonic and myeloarchitectonic study of the insular cortex of the bull, Bos taurus. Acta Histochem 110:245–255CrossRefPubMed

Salazar I, Ruiz Pesini P, Troconiz PF, Soriano JG, Alvarez PF (1988) The neocortex of the dog. 1. A classical cytoarchitectonic map. Anat Histol Embryol 17:169–187CrossRefPubMed

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

Seeley WW (2010) Anterior insula degeneration in frontotemporal dementia. Brain Struct Funct 214(5–6). doi:10.1007/s00429-010-0263-z (this issue)

Seeley WW, Allman JM, Carlin DA, Crawford RK, Macedo MN, Greicius MD, Dearmond SJ, Miller BL (2007) Divergent social functioning in behavioral variant frontotemporal dementia and Alzheimer disease: reciprocal networks and neuronal evolution. Alzheimer Dis Assoc Disord 21:S50–S57CrossRefPubMed

Sheffield G, Fay FH, Feder H, Kelly BP (2001) Laboratory digestion of prey and interpretation of walrus stomach contents. Mar Mam Sci 17:310–330CrossRef

Shelley BP, Trimble MR (2004) The insular lobe of Reil—its anatomico-functional, behavioural and neuropsychiatric attributes in humans—a review. World J Biol Psychiatry 5:176–200CrossRefPubMed

Showers MJ, Lauer EW (1961) Somatovisceral motor patterns in the insula. J Comp Neurol 117:107–115CrossRefPubMed

Singer T, Critchley HD, Preuschoff K (2009) A common role of insula in feelings, empathy and uncertainty. Trends Cogn Sci 13:334–340CrossRefPubMed

Stephan E, Pardo JV, Faris PL, Hartman BK, Kim SW, Ivanov EH, Daughters RS, Costello PA, Goodale RL (2003) Functional neuroimaging of gastric distention. J Gastrointest Surg 7:740–749CrossRefPubMed

Stevens CE, Hume ID (1995) Comparative physiology of the vertebrate digestive system, 2nd edn. Cambridge University Press, New York

Taylor S, Semionowicz DA, Davis KD (2009) Two systems of resting state connectivity between insula and cingulate cortex. Hum Brain Mapp 30:2731–2745CrossRefPubMed

Turner BH, Mishkin M, Knapp M (1980) Organization of the amygdalopetal projections from modality-specific cortical associations areas in the monkey. J Comp Neurol 191:515–543CrossRefPubMed

Vjacheslav GA, Bagaev VA, Nozdrachev AD, Panteleev SS (1996) Identification of gastric related neurons in the rat insular cortex. Neurosci Lett 216:5–8CrossRef

von Economo C (1926) Eine neue Art Spezialzellen des Lobus cinguli and Lobus insulae. Zschr ges Neurol Psychiat 100:706–712CrossRef

von Economo C (1927) L’architecture cellulaire normale de l’écorce cérébrale. Masson, Paris, pp 91–97

von Economo C, Koskinas GN (1925) Die Cytoarchitectonic der Hirnrinde des erwachsenen Menschen. Springer, Berlin

Voronov VA, Krasnoshchekova EI, Stotsman IM, Figurina II (1985) Morphofunctional organization and cortical projections of the medial geniculate body in the dolphin Phocoena phocoena. Zh Evol Biokhim Fiziol 21:55–60

Yaxley S, Rolls ET, Sienkiewicz ZJ (1990) Gustatory responses of single neurons in the insula of the macaque monkey. J Comp Neurol 63:689–700

Title: The insular cortex: a comparative perspective
Authors: Camilla Butti
Patrick R. Hof
Publication date: 01-06-2010
Publisher: Springer-Verlag
Published in: Brain Structure and Function / Issue 5-6/2010
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-010-0264-y

Keynote webinar | Spotlight on medication adherence

Springer Medicine

The insular cortex: a comparative perspective

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 5-6/2010

Conjoint activity of anterior insular and anterior cingulate cortex: awareness and response

Role of the anterior insula in task-level control and focal attention

Saliency, switching, attention and control: a network model of insula function

Interoception in anxiety and depression

The sentient self

A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis