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

Brain Structure and Function - Tập 214 Số 5-6 - Trang 495-517 - 2010
John M. Allman1, Nicole A. Tetreault1, Atiya Y. Hakeem1, Kebreten F. Manaye2, Katerina Semendeferi3, Joseph Erwin4, Soyoung Park1, Virginie Goubert1, Patrick R. Hof5
1Division of Biology 216-76, California Institute of Technology, Pasadena, CA 91125 USA
2Department of Physiology and Biophysics, College of Medicine, Howard University, Washington, DC 20059 USA
3Department of Anthropology, University of California, San Diego, La Jolla, CA, 92093, USA
4Biomedical Sciences and Pathobiology, Virginia Polytechnic Institute, Blackburg, VA, 24036, USA
5Department of Neuroscience, Mount Sinai School of Medicine, New York, NY 10029, USA

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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 90:118–122

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 935:107–117

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

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

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

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 134:392–403

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 11:1891–1898

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

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

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

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 515:243–259

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

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

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

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

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 274:2801–2810

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

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

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

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 28:8854–8866

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 5:303–305

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 65:63–74

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 104:11073–11078

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 130:1146–1158

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

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 4:385–390

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 18:932–948

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 66:132–140

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 4:233–243

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 15:3024–3033

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

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

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:e2939

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 60:1–42

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 116:479–489

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

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

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

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 104:20084–20089

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 104:19220–19225

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 50:506–517

Lombardo MV, Barnes JL, Wheelwright SJ, Baron-Cohen S (2007) Self-referential cognition and empathy in autism. PLoS One 2:e883

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 51:431–445

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

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

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

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 457:66–70

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

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 355:27–37

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 96:5268–5273

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 42:1727–1732

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 165–176

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 8:287–299

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 389:495–498

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 27:11012–11924

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

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 129:2945–2956

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 46:1265–1266

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

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 300:1755–1758

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

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

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 60:660–667

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–S57

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 106:129–155

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 66:888–896

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 63:82–106

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

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 48:43–50

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

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 118:673–684

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 303:1157–1162

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

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

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

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 105:12569–12574

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

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 15:1820–1826

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

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

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 100:706–712

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 28:4047–4056

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 11:868–877

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

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

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

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):179–202

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 69:1424–1433