Top

Published in:

Open Access 01-06-2010 | Original article

The von Economo neurons in frontoinsular and anterior cingulate cortex in great apes and humans

Authors: John M. Allman, Nicole A. Tetreault, Atiya Y. Hakeem, Kebreten F. Manaye, Katerina Semendeferi, Joseph M. Erwin, Soyoung Park, Virginie Goubert, Patrick R. Hof

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

Abstract

The von Economo neurons (VENs) are large bipolar neurons located in frontoinsular (FI) and anterior cingulate cortex in great apes and humans, but not other primates. We performed stereological counts of the VENs in FI and LA (limbic anterior, a component of anterior cingulate cortex) in great apes and in humans. The VENs are more numerous in humans than in apes, although one gorilla approached the lower end of the human range. We also examined the ontological development of the VENs in FI and LA in humans. The VENs first appear in small numbers in the 36th week post-conception, are rare at birth, and increase in number during the first 8 months after birth. There are significantly more VENs in the right hemisphere than in the left in FI and LA in postnatal brains of apes and humans. This asymmetry in VEN numbers may be related to asymmetries in the autonomic nervous system. The activity of the inferior anterior insula, which contains FI, is related to physiological changes in the body, decision-making, error recognition, and awareness. The VENs appear to be projection neurons, although their targets are unknown. We made a preliminary study of the connections of FI cortex based on diffusion tensor imaging in the brain of a gorilla. The VEN-containing regions connect to the frontal pole as well as to other parts of frontal and insular cortex, the septum, and the amygdala. It is likely that the VENs in FI are projecting to some or all of these structures and relaying information related to autonomic control, decision-making, or awareness. The VENs selectively express the bombesin peptides neuromedin B (NMB) and gastrin releasing peptide (GRP) which are also expressed in another population of closely related neurons, the fork cells. NMB and GRP signal satiety. The genes for NMB and GRP are expressed selectively in small populations of neurons in the insular cortex in mice. These populations may be related to the VEN and fork cells and may be involved in the regulation of appetite. The loss of these cells may be related to the loss of satiety signaling in patients with frontotemporal dementia who have damage to FI. The VENs and fork cells may be morphological specializations of an ancient population of neurons involved in the control of appetite present in the insular cortex in all mammals. We found that the protein encoded by the gene DISC1 (disrupted in schizophrenia) is preferentially expressed by the VENs. DISC1 has undergone rapid evolutionary change in the line leading to humans, and since it suppresses dendritic branching it may be involved in the distinctive VEN morphology.

Allman JM (2000) Evolving brains. Scientific American Library-W.H.Freeman, New York

Allman J, McLaughlin T, Hakeem A (1993) Brain weight and life-span in primate species. Proc Natl Acad Sci USA 90:118–122PubMedCrossRef

Allman JM, Hakeem A, Erwin JM, Nimchinsky E, Hof P (2001) Anterior cingulate cortex: the evolution of an interface between emotion and cognition. Ann NY Acad Sci 935:107–117PubMed

Allman J, Hakeem A, Watson K (2002) Two phylogenetic specializations in the human brain. Neuroscientist 8:335–346PubMedCrossRef

Allman J, Watson K, Tetreault N, Hakeem A (2005) Intuition and autism: a possible role for von Economo neurons. Trends Cogn Sci 9:367–373PubMedCrossRef

Aziz-Zadeh L, Kaplan J, Iocoboni M (2009) “Aha”: the neural correlates of verbal insight solutions. Hum Brain Mapp 30:908–916PubMedCrossRef

Barger N, Stefanacci L, Semendeferi K (2007) A comparative volumetric analysis of the amygdaloid complex and basolateral division in the human and ape brain. Am J Phys Anthropol 134:392–403PubMedCrossRef

Baron-Cohen S, Ring HA, Wheelwright S, Bullmore ET, Brammer MJ, Simmons A, Williams SC (1999) Social intelligence in the normal and autistic brain: an fMRI study. Eur J Neurosci 11:1891–1898PubMedCrossRef

Bartels A, Zeki S (2004) The neural correlates of maternal and romantic love. Neuroimage 21:1155–1166PubMedCrossRef

Bass AH, Gilland EH, Baker R (2008) Evolutionary origins for social vocalization in a vertebrate hindbrain-spinal compartment. Science 321:417–421PubMedCrossRef

Berthoz S, Armony JL, Blair RJR, Dolan RJ (2002) An fMRI study of intentional and unintentional (embarrassing) violations of social norms. Brain 125:1696–1708PubMedCrossRef

Betz W (1881) Ueber die feinere Structur der Gehirnrinde des Menschen. Zentralbl Med Wiss 19:193–195, 209–213, 231–234

Brauer K, Schober W (1970) Catalogue of mammalian brains. VEB Gustav Fischer Verlag, Jena

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 515:243–259PubMedCrossRef

Chubb JE, Bradshaw NJ, Soares DC, Porteous DJ, Millar JK (2008) The DISC locus in psychiatric illness. Mol Psychiatry 13:36–64PubMedCrossRef

Craig AD (2003) A new view of pain as a homeostasis emotion. Trends Neurosci 26:303–307PubMedCrossRef

Craig AD (2005) Forebrain emotional asymmetry: a neuroanatomical basis? Trends Cogn Sci 912:566–571CrossRef

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

Craig AD (2010) The sentient self. Brain Struct Funct. doi:10.1007/s00429-010-0248-y

Crespi B, Summers K, Dorus S (2007) Adaptive evolution of genes underlying schizophrenia. Proc Roy Soc B 274:2801–2810CrossRef

Critchley HD, Elliott R, Mathias CJ, Dolan RJ (2000) Neural activity relating to generation and representation of galvanic skin conductance responses. J Neurosci 20:3033–3040PubMed

Critchley HD, Mathias C, Dolan R (2001a) Neural activity in the human brain relating to uncertainty and arousal during anticipation. Neuron 29:537–545PubMedCrossRef

Critchley HD, Melmed RN, Featherstone E, Mathias CJ, Dolan RJ (2001b) Brain activity during biofeedback relaxation: a functional neuroimaging investigation. Brain 124:1003–1012PubMedCrossRef

Croxson PL, Johansen-Berg H, Behrens TE, Robson MD, Pinsk MA, Gross CG, Richter W, Richter MC, Kastner S, Rushworth MF (2005) Quantitative investigation of connections of the prefrontal cortex in the human and macaque using probabilistic diffusion tractography. J Neurosci 28:8854–8866CrossRef

Damasio A (1994) Descartes error. Putnam, New York

Dehaene S, Posner MI, Tucker DM (1994) Localization of a neural system for error detection and compensation. Psychol Sci 5:303–305CrossRef

Di Martino A, Ross K, Uddin L, Sklar A, Castellanos F, Milham M (2009) Processes in autism spectrum disorders: an activation likelihood estimation meta-analysis. Biol Psychiatry 65:63–74PubMedCrossRef

Dosenbach NU, Fair DA, Miezin FM, Cohen AL, Wenger KK, Dosenbach RA, Fox MD, Snyder AZ, Vincent JL, Raichle ME, Schlaggar BL, Petersen SE (2007) Distinct brain networks for adaptive and stable task control in humans. Proc Natl Acad Sci USA 104:11073–11078PubMedCrossRef

Duan X, Chang JH, Ge S, Faulkner RL, Kim JY, Kitabatake Y, Liu XB, Yang CH, Jordan JD, Ma DK, Liu CY, Ganesan S, Cheng HJ, Ming GL, Lu B, Song H (2007) Disrupted-in-schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell 130:1146–1158PubMedCrossRef

Galdikas BMF (1985) Orangutan sociality at Tanjung Puting. Am J Primatol 9:101–119CrossRef

Gallyas F (1971) A principle for silver staining of tissue elements by physical development. Acta Morphol Acad Sci 19:57–71

Gehring WJ, Goss B, Coles MGH, Meyer DE, Donchin E (1993) A neural system of error detection and compensation. Psychol Sci 4:385–390CrossRef

Gilbert S, Spengler S, Simons J, Steele J, Lawrie S, Frith C, Burgess P (2006) Functional specialization within rostral prefrontal cortex (Area 10): a meta-analysis. J Cogn Neurosci 18:932–948PubMedCrossRef

Gilles FH, Leviton A, Dooling EC (1983) Developing human brain, growth and epidemiologic neuropathology. John Wright - PSG Inc, Boston

Gündel H, López-Sala A, Ceballos-Baumann AO, Deus J, Cardoner N, Marten-Mittag B, Soriano-Mas C, Pujol J (2004) Alexithymia correlates with the size of right anterior cingulate. Psychosom Med 66:132–140PubMedCrossRef

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

Hammarberg C (1895) Studien über Klinik und Pathologie der Idiotie nebst Untersuchungen über die normale Anatomie des Hirnrinde. Berling, Uppsala

Harrison NA, Gray MA, Critchley HD (2009) Dynamic pupillary exchange engages brain regions encoding social salience. Soc Neurosci 4:233–243PubMedCrossRef

Hashimoto R, Numakawa T, Ohnishi T, Kumamaru E, Yagasaki Y, Ishimoto T, Mori T, Nemoto K, Adachi N, Izumi A, Chiba S, Noguchi H, Suzuki T, Iwata N, Ozaki N, Taguchi T, Kamiya A, Kosuga A, Tatsumi M, Kamijima K, Weinberger DR, Sawa A, Kunugi H (2006) Impact of the DISC1 Ser704Cys polymorphism on risk for major depression, brain morphology and ERK signaling. Hum Mol Genet 15:3024–3033PubMedCrossRef

Hayashi M, Ito M, Shimizu K (2001) The spindle neurons are present in the cingulate cortex of chimpanzee fetus. Neurosci Lett 309:97–100PubMedCrossRef

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

Houdé O, Rossi S, Lubin A, Joliot M (2010) Mapping numerical processing, reading, and executive functions in the developing brain: an fMRI meta-analysis of 52 studies including 842 children. Dev Sci 1:1–10

Jabbi M, Bastiaansen J, Keysers C (2008) A common anterior insula representation of disgust observation, experience and imagination shows divergent functional connectivity pathways. PLos One 8:e2939CrossRef

Jensen RT, Battey JF, Spindel ER, BEnya RV (2008) International Union of Pharmacology, LXVIII. Mammalian bombesin receptors: nomenclature, distribution, pharmacology, signaling, and functions in normal and disease states. Pharmacol Rev 60:1–42PubMedCrossRef

Kaufman JA, Paul LK, Manaye KF, Granstedt AE, Hof PR, Hakeem AY, Allman JM (2008) Selective reduction of Von Economo neuron number in agenesis of the corpus callosum. Acta Neuropathol 116:479–489PubMedCrossRef

Kennedy DP, Semendeferi K, Courchesne E (2007) No reduction of spindle neuron number in frontoinsular cortex in autism. Brain Cogn 64:124–129PubMedCrossRef

Kikyo H, Ohki K (2002) Neural correlates for feeling-of-knowing: an fMRI parametric analysis. Neuron 36:177–186PubMedCrossRef

Klein TA, Endrass T, Kathmann N, Neumann J, von Cramon DY, Ullsperger M (2007) Neural correlates of error awareness. NeuroImage 34:1774–1781PubMedCrossRef

Krueger F, McCabe K, Moll J, Kriegeskorte N, Zahn R, Strenziok M, Heinecke A, Grafman J (2007) Neural correlates of trust. Proc Natl Acad Sci USA 104:20084–20089PubMedCrossRef

Kunimatsu Y, Nakatsukasa M, Sawada Y, Sakai T, Hyodo M, Hyodo H, Itaya T, Nakaya H, Saegusa H, Mazurier A, Saneyoshi M, Tsujikawa H, Yamamoto A, Mbua E (2007) A new Late Miocene great ape from Kenya and its implications for the origins of African great apes and humans. Proc Natl Acad Sci USA 104:19220–19225PubMedCrossRef

Lamm C, Singer T (2010) Role of anterior insular cortex in social emotions. Brain Struct Funct. doi:10.1007/s00429-010-0251-3

Lim M, Young L (2006) Neuropeptidergic regulation of affiliative behavior and social bonding in animals. Horm Behav 50:506–517PubMedCrossRef

Lombardo MV, Barnes JL, Wheelwright SJ, Baron-Cohen S (2007) Self-referential cognition and empathy in autism. PLoS One 2:e883PubMedCrossRef

Lorberbaum JP, Newman JD, Horwitz AR, Dubno JR, Lydiard RB, Hamner MB, Bohning DE, George MS (2002) A potential role for thalamocingulate circuitry in human maternal behavior. Biol Psychiatry 51:431–445PubMedCrossRef

MacNeilage PF, Rogers LJ, Vallortigara G (2009) Origins of the left & right brain. Sci Am 301:60–67PubMedCrossRef

Merker B (1983) Silver staining of cell bodies by means of physical development. J Neurosci Methods 9:235–241PubMedCrossRef

Mitani JC, Grether GF, Rodman PS, Priatna D (1991) Associations among wild orangutans: sociality, passive aggregations or chance? Anim Behav 42:33–46CrossRef

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

Naqvi NH, Bechara A (2009) The hidden island of addiction: the insula. Trends Neurosci 32:56–67PubMedCrossRef

Nelson S, Dosenbach, N, Cohen, A, Schlaggar B, Petersen S (2010) Role of the anterior insula in task-level control and focal attention. Brain Struct Funct. doi:10.1007/s00429-010-0260-2

Ngowyang G (1932) Beschreibung einer Art von Spezialzellen in der Inselrinde - zugleich Bemerkungen über die v. Economoschen Spezialzellen. J Psychol Neurol 44:671–674

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

Nimchinsky E, Gilissen E, Allman J, Perl D, Erwin J, Hof P (1999) A neuronal morphologic type unique to humans and great apes. Proc Nat Acad Sci USA 96:5268–5273PubMedCrossRef

Numan R (2000) The behavioral neuroscience of the septal region. Springer, New York

Oppenheimer SM, Gelb A, Girvin JP, Hachinski VC (1992) Cardiovascular effects of human insular cortex stimulation. Neurology 42:1727–1732PubMed

Patterson F, Gordon W (2002) Twenty-seven years of Project Koko and Michael. In: Galdikas B, Briggs N, Sheeran L, Shapiro G, Goodall J (eds) All apes great and small, vol I. Kluwer Press, New York, pp 165–176CrossRef

Paul LK, Brown WS, Adolphs R, Tyszka JM, Richards LJ, Mukherjee P, Sherr EH (2007) Agenesis of the corpus callosum: genetic, developmental and functional aspects of connectivity. Nat Rev Neurosci 8:287–299PubMedCrossRef

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

Ploran E, Nelson S, Velanova K, Petersem S, Wheeler M (2007) Evidence accumulation and moment of recognition: dissociating perceptual recognition processes using fMRI. J Neurosci 27:11012–11924CrossRef

Preuschhoff K, Quartz S, Bossaerts P (2008) Human insula activation reflects risk prediction errors as well as risk. J Neurosci 28:2745–2752CrossRef

Ramón y Cajal S (1899) Textura del Sistema Nervioso del Hombre y de los Vertebrados, Tomo II. Nicolás Moya, Madrid

Rankin KP, Gorno-Tempini ML, Allison SC, Stanley CM, Glenn S, Weiner MW, Miller BL (2006) Structural anatomy of empathy in neurodegenerative disease. Brain 129:2945–2956PubMedCrossRef

Rilling J, Goldsmith D, Glenn A, Jairam M, Elfenbein H, Dagenais J, Murdock C, Pagnoni (2008) Neural correlates of the affective response to unreciprocated cooperation. Neuropsychologia 46:1265–1266CrossRef

Rogers L, Andrew R (2002) Comparative vertebrate lateralization. Cambridge University Press, CambridgeCrossRef

Rose M (1927) Gyrus limbicus anterior und Regio retrosplenialis (Cortex holoprotoptychos quinquestratificatus) - Vergleichende Architektonik bei Tier und Menschen. J Psychol Neurol 35:5–217

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

Sanfey AG, Rilling RJ, Aronson JA, Nystrom LE, Cohen JD (2003) The neural basis of economic decision-making in the ultimatum game. Science 300:1755–1758PubMedCrossRef

Schenker NM, Desgouttes A, Semendeferi K (2005) Neural connectivity and cortical substrates of cognition in hominoids. J Hum Evol 49:547–569PubMedCrossRef

Seeley WW (2008) Selective functional, regional, and neuronal vulnerability in frontotemporal dementia. Curr Opin Neurol 21:701–707PubMedCrossRef

Seeley WW, Carlin DA, Allman JM, Macedo MN, Bush C, Miller BL, Dearmond SJ (2006) Early frontotemporal dementia targets neurons unique to apes and humans. Ann Neurol 60:660–667PubMedCrossRef

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–S57PubMedCrossRef

Semendeferi K, Armstrong E, Schleicher A, Zilles K, Van Hoesen GW (1998) Limbic frontal cortex in hominoids: a comparative study of area 13. Am J Phys Anthropol 106:129–155PubMedCrossRef

Shaw P, Lalonde F, Lepage C, Rabin C, Eckstrand K, Sharp W, Greenstein D, Evans A, Giedd JM, Rapoport J (2009) Development of cortical asymmetry in typically developing children and its disruption in attention-deficit/hyperactivity disorder. Arch Gen Psychiatry 66:888–896PubMedCrossRef

Sherwood CC, Holloway RL, Erwin JM, Hof PR (2004) Cortical orofacial motor representation in Old World monkeys, great apes, and humans. II: stereologic analysis of chemoarchitecture. Brain Behav Evol 63:82–106PubMedCrossRef

Sherwood CC, Wahl E, Erwin JM, Hof PR, Hopkins WD (2007) Histological asymmetries of primary motor cortex predict handedness in chimpanzees. J Comp Neurol 503:525–537PubMedCrossRef

Shin LM, Dougherty DD, Orr SP, Pitman RK, Lasko M, Macklin ML, Alpert NM, Fischman AJ, Rauch SL (2000) Activation of anterior paralimbic structures during guilt-related script-driven imagery. Biol Psychiatry 48:43–50PubMedCrossRef

Shorvon S (2005) Handbook of epilepsy treatment. Wiley, New YorkCrossRef

Simms ML, Kemper TL, Timbie CM, Bauman ML, Blatt GJ (2009) The anterior cingulate cortex in autism: heterogeneity of qualitative and quantitative cytoarchitectonic features suggests possible subgroups. Acta Neuropathol 118:673–684PubMedCrossRef

Singer T, Seymour B, O’Doherty J, Kaube H, Dolan RJ, Frith CD (2004a) Empathy for pain involves the affective but not sensory components of pain. Science 303:1157–1162PubMedCrossRef

Singer T, Kiebel SJ, Winston JS, Dolan RJ, Frith CD (2004b) Brain responses to the acquired moral status of faces. Neuron 41:653–662PubMedCrossRef

Singleton I, van Schaik CP (2002) The social organisation of a population of Sumatran orangutans. Folia Primatol 73:1–20PubMedCrossRef

Spence SA, Farrow TF, Herford AE, Wilkinson ID, Zheng Y, Woodruff PW (2001) Behavioural and functional anatomical correlates of deception in humans. NeuroReport 12:2849–2853PubMedCrossRef

Sridharan D, Levitin DJ, Menon V (2008) A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proc Natl Acad Sci USA 105:12569–12574PubMedCrossRef

Stephan H, Frahm HD, Baron G (1981) New and revised data on volumes of brain structures in insectivores and primates. Folia Primatol 35:1–29PubMedCrossRef

Szebenyi G, Bollati F, Bisbal M, Sheridan S, Faas L, Wray R, Haferkamp S, Nguyen S, Caceres A, Brady S (2005) Activity-driven dendritic remodeling requires microtubule-associated Protein 1a. Curr Biol 15:1820–1826PubMedCrossRef

Ullsperger M, von Cramon DY (2004) Neuroimaging of performance monitoring: error detection and beyond. Cortex 40:593–604PubMedCrossRef

Uylings H, Jacosen A, Zilles K, Amunts K (2006) Left-right asymmetry in volume and number of neurons in adult Broca’s area. Cortex 42:652–658PubMedCrossRef

van Kooten (2008) Autism counts. Dissertation, Maastricht University

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

Von Economo C (2009) Cellular structure of the human cerebral cortex. Translated by L.C. Triarhou, Karger, Basel

Von Economo C, Koskinas G (1925) Die Cytoarchitectonik der Hirnrinde des erwachsenen Menschen. Springer, Berlin

Wang SS, Shultz JR, Burish MJ, Harrison KH, Hof PR, Towns LC, Wagers MW, Wyatt KD (2008) Functional trade-offs in white matter axonal scaling. J Neurosci 28:4047–4056PubMedCrossRef

Watkins KE, Paus T, Lerch JP, Zijdenbos A, Collins DL, Neelin P, Taylor J, Worsley KJ, Evans AC (2001) Structural asymmetries in human brain: a voxel-based statistical analysis of 142 brains. Cereb Cortex 11:868–877PubMedCrossRef

Watson KK, Jones TK, Allman JM (2006) Dendritic architecture of the von Economo neurons. Neuroscience 141:1107–1112PubMedCrossRef

Watson KK, Matthews BJ, Allman JM (2007) Brain activation during sight gags and language-dependent humor. Cereb Cortex 17:314–324PubMedCrossRef

Welker WI, Seidenstein S (1959) Somatic sensory representation in the cerebral cortex of the raccoon (Procyon lotor). J Comp Neurol 111:469–501PubMedCrossRef

Williamson P, Allman JM (2010) The human illnesses: neuropsychiatric disorders and the nature of the human brain. Oxford University Press (in press)

Wittling W (1995) Brain Asymmetry in the control of autonomic-physiological activity. In: Davidson RJ, Hugdahl K (eds) Brain asymmetry. MIT Press, Cambridge, pp 305–356

Woodward J, Allman J (2007) Moral intuition: its neural substrates and normative significance. J Physiol Paris 101(4–6):179–202PubMedCrossRef

Woolley JD, Gorno-Tempini ML, Seeley WW, Rankin K, Lee SS, Matthews BR, Miller BL (2007) Binge eating is associated with right orbitofrontal-insular-striatal atrophy in frontotemporal dementia. Neurology 69:1424–1433PubMedCrossRef

Title: The von Economo neurons in frontoinsular and anterior cingulate cortex in great apes and humans
Authors: John M. Allman
Nicole A. Tetreault
Atiya Y. Hakeem
Kebreten F. Manaye
Katerina Semendeferi
Joseph M. Erwin
Soyoung Park
Virginie Goubert
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/s00429-010-0254-0

At a glance: The STEP trials

Springer Medicine

The von Economo neurons in frontoinsular and anterior cingulate cortex in great apes and humans

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 5-6/2010

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

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

The role of anterior insular cortex in social emotions

Anterior insula activations in perceptual paradigms: often observed but barely understood

The insula and drug addiction: an interoceptive view of pleasure, urges, and decision-making

Once an island, now the focus of attention