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Comparison of bonobo and chimpanzee brain microstructure reveals differences in socio-emotional circuits

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Abstract

Despite being closely related, bonobos and chimpanzees exhibit several behavioral differences. For instance, studies indicate that chimpanzees are more aggressive, territorial, and risk-taking, while bonobos exhibit greater social tolerance and higher rates of socio-sexual interactions. To elucidate the potential neuroanatomical variation that accompanies these differences, we examined the microstructure of selected brain areas by quantifying the neuropil fraction, a measure of the relative tissue area occupied by structural elements of connectivity (e.g., dendrites, axons, and synapses) versus cell bodies. In bonobos and chimpanzees, we compared neuropil fractions in the nucleus accumbens (NAc; core and shell), amygdala (whole, accessory basal, basal, central and lateral nuclei), anterior cingulate cortex (ACC; dorsal and subgenual), anterior insular cortex (AIC), and primary motor cortex (M1). In the dorsal ACC and frontoinsular cortex (FI) we also quantified numbers of von Economo neurons (VENs), a unique subset of neurons thought to be involved in rapid information processing during social interactions. We predicted that the neuropil fraction and number of VENs in brain regions associated with socio-emotional processing would be higher in bonobos. In support of this hypothesis, we found that bonobos had significantly greater neuropil in the central and accessory basal nuclei of the amygdala, as well as layers V–VI of the subgenual ACC. However, we did not find a difference in the numbers of VENs between the two species. These findings support the conclusion that bonobo and chimpanzee brains differ in the anatomical organization of socio-emotional systems that may reflect species-specific variation in behavior.

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References

  • Aggleton JP (1992) The functional effects of amygdala lesions in humans: a comparison with findings from monkeys. In: Aggleton JP (ed) The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction. Wiley-Liss, New York, pp 485–503

    Google Scholar 

  • Aggleton JP, Mishkin M (1986) The amygdala: sensory gateway to the emotions. In: Plutchik R, Kellerman H (eds) Emotion: theory, research and experience, vol 3. Academic Press, Orlando, pp 281–299

    Google Scholar 

  • Alexander-Bloch AF, Gogtay N, Meunier D, Birn R, Clasen L, Lalonde F, Lenroot R, Giedd J, Bullmore ET (2010) Disrupted modularity and local connectivity of brain functional networks in childhood-onset schizophrenia. Front Syst Neurosci 4:147

    Article  PubMed  PubMed Central  Google Scholar 

  • Allman JM, Hakeem A, Erwin JM, Nimchinsky E, Hof PR (2001) The anterior cingulate cortex. Ann N Y Acad Sci 935:107–117

    Article  CAS  PubMed  Google Scholar 

  • Allman JM, Watson KK, Tetreault NA, Hakeem AY (2005) Intuition and autism: a possible role for von Economo neurons. Trends Cogn Sci 9:367–373

    Article  PubMed  Google Scholar 

  • Allman JM, Tetreault NA, Hakeem AY, Manaye KF, Semendeferi K, Erwin JM, Park S, Goubert V, Hof PR (2010) The von Economo neurons in frontoinsular and anterior cingulate cortex in great apes and humans. Brain Struct Funct 214:495–517

    Article  PubMed  Google Scholar 

  • Amaral DG, Price JL (1984) Amygdalo-cortical projections in the monkey (Macaca fascicularis). J Comp Neurol 230:465–496

    Article  CAS  PubMed  Google Scholar 

  • Bales KL, Carter CS (2003) Sex differences and developmental effects of oxytocin on aggression and social behavior in prairie voles (Microtus ochrogaster). Horm Behav 44:178–184

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Barrot M, Olivier JDA, Perrotti LI et al (2002) CREB activity in the nucleus accumbens shell controls gating of behavioral responses to emotional stimuli. Proc Natl Acad Sci 99:11435–11440

    Article  CAS  PubMed  Google Scholar 

  • Bauernfeind AL, de Sousa AA, Avasthi T, Dobson SD, Raghanti MA, Lewandowski A, Zilles K, Semendeferi K, Allman JM, Craig AD, Hof PR, Sherwood CC (2013) A volumetric comparison of the insular cortex and its subregions in primates. J Hum Evol 64:263–279

    Article  PubMed  PubMed Central  Google Scholar 

  • Behringer V, Deschner T, Murtagh R, Stevens JMG, Hohmann G (2014) Age-related changes in thyroid hormone levels of bonobos and chimpanzees indicate heterochrony in development. J Hum Evol 66:83–88

    Article  PubMed  Google Scholar 

  • Boesch C, Boesch-Achermann H (2000).The chimpanzees of the taï forest. Behavioural ecology and evolution. Boesch C, Boesch-Achermann H (eds), Oxford University Press New York. p 316

    Google Scholar 

  • Bosch OJ, Neumann ID (2012) Both oxytocin and vasopressin are mediators of maternal care and aggression in rodents: from central release to sites of action. Horm Behav 61:293–303

    Article  CAS  PubMed  Google Scholar 

  • Brüne M, Schöbel A, Karau R, Benali A, Faustmann PM, Juckel G, Petrasch-Parwez E (2010) Von Economo neuron density in the anterior cingulate cortex is reduced in early onset schizophrenia. Acta Neuropathol 119:771–778

    Article  PubMed  Google Scholar 

  • Butler RK, Ehling S, Barbar M et al (2017) Distinct neuronal populations in the basolateral and central amygdala are activated with acute pain, conditioned fear, and fear-conditioned analgesia. Neurosci Lett 661:11–17

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Butti C, Santos M, Uppal N, Hof PR (2013) Von economo neurons: clinical and evolutionary perspectives. Cortex 49(1):312–326

    Article  PubMed  Google Scholar 

  • Butti C, Ewan Fordyce R, Raghanti MA, Gu X, Bonar CJ, Wicinski BA, Wong EW, Roman J, Brake A, Eaves E, Spocter MA, Tang CY, Jacobs B, Sherwood CC, Hof PR (2014) The cerebral cortex of the Pygmy Hippopotamus, (Cetartiodactyla, Hippopotamidae): MRI, cytoarchitecture, and neuronal morphology. Anat Rec 297(4):670–700

    Article  Google Scholar 

  • Campbell A (2008) Attachment, aggression and affiliation: the role of oxytocin in female social behavior. Biol Psychol 77:1–10

    Article  PubMed  Google Scholar 

  • Campbell-Smith EJ, Holmes NM, Lingawi NW et al (2015) Oxytocin signaling in basolateral and central amygdala nuclei differentially regulates the acquisition, expression, and extinction of context-conditioned fear in rats. Learn Mem 22:247–257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Casanova MF, Buxhoeveden DP, Switala AE, Roy E (2002) Minicolumnar pathology in autism. Neurology 58:428–432

    Article  PubMed  Google Scholar 

  • Casanova MF, van Kooten IAJ, Switala AE et al (2006) Minicolumnar abnormalities in autism. Acta Neuropathol 112:287–303

    Article  PubMed  Google Scholar 

  • Clay Z, Archbold J, Zuberbühler K (2015) Functional flexibility in wild bonobo vocal behaviour. PeerJ 3:e1124

    Article  PubMed  PubMed Central  Google Scholar 

  • Cobos I, Seeley WW (2013) Human von Economo neurons express transcription factors associated with layer V subcerebral projection neurons. Cereb Cortex 25:213–220

    Article  PubMed  PubMed Central  Google Scholar 

  • Cole BJ, Robbins TW (1989) Effects of 6-hydroxydopamine lesions of the nucleus accumbens septi on performance of a 5-choice serial reaction time task in rats: implications for theories of selective attention and arousal. Behav Brain Res 33:165–179

    Article  CAS  PubMed  Google Scholar 

  • Courchesne E, Pierce K (2005) Why the frontal cortex in autism might be talking only to itself: local over-connectivity but long-distance disconnection. Curr Opin Neurobiol 15:225–230

    Article  CAS  PubMed  Google Scholar 

  • Craig AD (2005) Forebrain emotional asymmetry: a neuroanatomical basis? Trends Cogn Sci 9:566–571

    Article  PubMed  Google Scholar 

  • Dajani DR, Uddin LQ (2016) Local brain connectivity across development in autism spectrum disorder: a cross-sectional investigation. Autism Res 9:43–54

    Article  PubMed  Google Scholar 

  • Davis M (1992) The role of the amygdala in fear and anxiety. Annu Rev Neurosci 15:353–375

    Article  CAS  PubMed  Google Scholar 

  • De Waal FM (1988) The communicative repertoire of captive bonobos (Pan paniscus), compared to that of chimpanzees. Behav 106:183–251

    Article  Google Scholar 

  • Delgado RA, Van Schaik CP (2000) The behavioral ecology and conservation of the orangutan (Pongo pygmaeus): a tale of two islands. Evol Anthropol 9:201–218

    Article  Google Scholar 

  • Devinsky O, Morrell MJ, Vogt BA (1995) Contributions of anterior cingulate cortex to behaviour. Brain 118:279–306

    Article  PubMed  Google Scholar 

  • Dijkstra AA, Lin L-C, Nana AL et al (2018) Von Economo neurons and fork cells: a neurochemical signature linked to monoaminergic function. Cereb Cortex 28:131–144

    Article  Google Scholar 

  • Donaldson ZR, Kondrashov FA, Putnam A, Bai Y, Stoinski TL, Hammock EAD, Young LJ (2008) Evolution of a behavior-linked microsatellite-containing element in the 5′ flanking region of the primate AVPR1A gene. BMC Evol Biol 8:180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duerden EG, Arsalidou M, Lee M, Taylor MJ (2013) Lateralization of affective processing in the insula. NeuroImage 78:159–175

    Article  PubMed  Google Scholar 

  • Etkin A, Egner T, Kalisch R (2011) Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn Sci 15:85–93

    Article  PubMed  Google Scholar 

  • Evrard HC, Forro T, Logothetis NK (2012) Von Economo neurons in the anterior insula of the macaque monkey. Neuron 74:482–489

    Article  CAS  Google Scholar 

  • Fadok JP, Markovic M, Tovote P, Lüthi A (2018) New perspectives on central amygdala function. Curr Opin Neurobiol 49:141–147

    Article  CAS  PubMed  Google Scholar 

  • Floresco SB (2015) The nucleus accumbens: an interface between cognition, emotion, and action. Annu Rev Psychol 66:25–52

    Article  PubMed  Google Scholar 

  • Friedman DP, Aggleton JP, Saunders RC (2002) Comparison of hippocampal, amygdala, and perirhinal projections to the nucleus accumbens: combined anterograde and retrograde tracing study in the Macaque brain. J Comp Neurol 450(4):345–365

    Article  PubMed  Google Scholar 

  • Furuichi T (1997) Agonistic interactions and matrifocal dominance rank of wild bonobos (pan paniscus) at wamba. Int J Primatol 18:855–875

    Article  Google Scholar 

  • Furuichi T (2011) Female contributions to the peaceful nature of bonobo society. Evol Anthropol 20:131–142

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Goodall J (1986) The Chimpanzees of Gombe: patterns of behavior. Harvard University Press, Cambridge

    Google Scholar 

  • Gray JR, Braver TS (2002) Personality predicts working-memory-related activation in the caudal anterior cingulate cortex. Cogn Affect Behav Neurosci 2:64–75

    Article  PubMed  Google Scholar 

  • Graziano M (2005) Arm movements evoked by electrical stimulation in the motor cortex of monkeys. J Neurophysiol 94:4209–4223

    Article  PubMed  Google Scholar 

  • Groenewegen HJ, Wright CI, Beijer AV (1996) The nucleus accumbens: gateway for limbic structures to reach the motor system? Prog Brain Res 107:485–511

    Article  CAS  PubMed  Google Scholar 

  • Gruber T, Clay Z (2016) A comparison between bonobos and chimpanzees: a review and update. Evol Anthropol 25:239–252

    Article  PubMed  Google Scholar 

  • Gruber T, Clay Z, Zuberbühler K (2010) A comparison of bonobo and chimpanzee tool use: evidence for a female bias in the Pan lineage. Anim Behav 80(6):1023–1033

    Article  Google Scholar 

  • Gu X, Hof PR, Friston KJ, Fan J (2013) Anterior insular cortex and emotional awareness. J Comp Neurol 521:3371–3388

    Article  PubMed  PubMed Central  Google Scholar 

  • Gundersen HJG, Jensen EBV, Kieu K et al (1999) The efficiency of systematic sampling in stereology—reconsidered. J Microsc 193:199–211

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Han W, Tellez LA, Rangel MJ, Motta SC, Zhang X, Perez IO, Canteras NS, Shammah-Lagnado SJ, van den Pol AN, de Araujo IE (2017) Integrated control of predatory hunting by the central nucleus of the amygdala. Cell 168(1–2):311–324.e18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hare B, Melis AP, Woods V, Hastings S, Wrangham R (2007) Tolerance allows bonobos to outperform chimpanzees on a cooperative task. Curr Biol 17:619–623

    Article  CAS  PubMed  Google Scholar 

  • Haun DBM, Nawroth C, Call J (2011) Great Apes’ risk-taking strategies in a decision making task. PLoS One 6(12):e28801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herrmann E, Hare B, Call J, Tomasello M (2010) Differences in the cognitive skills of bonobos and chimpanzees. PLoS One 5:2–5

    Google Scholar 

  • Herrmann E, Hare B, Cissewski J, Tomasello M (2011) A comparison of temperament in nonhuman apes and human infants. Dev Sci 14:1393–1405

    Article  PubMed  Google Scholar 

  • Heysieattalab S, Naghdi N, Zarrindast MR et al (2016) The effects of GABAAand NMDA receptors in the shell-accumbens on spatial memory of METH-treated rats. Pharmacol Biochem Behav 142:23–35

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Holdefer RN, Miller LE (2002) Primary motor cortical neurons encode functional muscle synergies. Exp Brain Res 146:233–243

    Article  CAS  PubMed  Google Scholar 

  • Holroyd CB, Nieuwenhuis S, Yeung N, Nystrom L, Mars RB, Coles MGH, Cohen JD (2004) Dorsal anterior cingulate cortex shows fMRI response to internal and external error signals. Nat Neurosci 7:497–498

    Article  CAS  PubMed  Google Scholar 

  • Hopkins WD, Lyn H, Cantalupo C (2009) Volumetric and lateralized differences in selected brain regions of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus). Am J Primatol 71:988–997

    Article  PubMed  PubMed Central  Google Scholar 

  • Hopkins WD, Donaldson ZR, Young LJ (2012) A polymorphic indel containing the RS3 microsatellite in the 5′ flanking region of the vasopressin V1a receptor gene is associated with chimpanzee (Pan troglodytes) personality. Genes Brain Behav 11:552–558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hopkins WD et al (2017) Social cognition and brain organization in chimpanzees (Pan troglodytes) and bonobos (Pan paniscus). In: Hare (ed) Bonobos: unique in mind, brain and behavior. Oxford University Press, B

    Google Scholar 

  • Hrybouski S, Aghamohammadi-Sereshki A, Madan CR et al (2016) Amygdala subnuclei response and connectivity during emotional processing. Neuroimage 133:98–110

    Article  PubMed  Google Scholar 

  • Ito R, Robbins TW, Pennartz CM, Everitt BJ (2008) Functional interaction between the hippocampus and nucleus accumbens shell is necessary for the acquisition of appetitive spatial context conditioning. J Neurosci 28:6950–6959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalin NH, Shelton SE, Davidson RJ (2004) The role of the central nucleus of the amygdala in mediating fear and anxiety in the primate. J Neurosci 24:5506–5515

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Kerfoot EC, Williams CL (2018) Contributions of the nucleus accumbens shell in mediating the enhancement in memory following noradrenergic activation of either the amygdala or hippocampus. Front Pharmacol 9:47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keverne EB, Curley JP (2004) Vasopressin, oxytocin and social behaviour. Curr Opin Neurobiol 14:777–783

    Article  CAS  PubMed  Google Scholar 

  • Kim EJ, Sidhu M, Gaus SE, Huang EJ, Hof PR, Miller BL, DeArmond SJ, Seeley WW (2011) Selective frontoinsular von Economo neuron and fork cell loss in early behavioral variant frontotemporal dementia. Cereb Cortex 22:251–259

    Article  PubMed  PubMed Central  Google Scholar 

  • Klumpp H, Angstadt M, Phan KL (2012) Insula reactivity and connectivity to anterior cingulate cortex when processing threat in generalized social anxiety disorder. Biol Psychol 89:273–276

    Article  PubMed  Google Scholar 

  • Knutson B, Adams CM, Fong GW, Hommer D (2001) Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J Neurosci 21:RC159

    Article  CAS  PubMed  Google Scholar 

  • Koski L, Paus T (2000) Functional connectivity of the anterior cingulate cortex within the human frontal lobe: a brain-mapping meta-analysis. Exp brain Res 133:55–65

    Article  CAS  PubMed  Google Scholar 

  • Lázaro-Muñoz G, LeDoux JE, Cain CK (2010) Sidman instrumental avoidance initially depends on lateral and basal amygdala and is constrained by central amygdala-mediated pavlovian processes. Biol Psychiatry 67:1120–1127

    Article  PubMed  PubMed Central  Google Scholar 

  • LeDoux J (2007) The amygdala. Curr Biol 17:868–874

    Article  CAS  Google Scholar 

  • LeDoux JE, Iwata J, Cicchetti P, Reis DJ (1988) Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J Neurosci 8:2517–2529

    Article  CAS  PubMed  Google Scholar 

  • LeDoux J, Ciocchetti P, Xagoraris A, Romanski L (1990) The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J Neurosci 10(4):1062–1069

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Wang ZX (2003) Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles. Neurosci 121:537–544

    Article  CAS  Google Scholar 

  • Lorberbaum JP, Newman JD, Horwitz AR et al (2002) A potential role for thalamocingulate circuitry in human maternal behavior. Biol Psychiatry 51:431–445

    Article  PubMed  Google Scholar 

  • Lovero KL, Simmons AN, Aron JL, Paulus MP (2009) Anterior insular cortex anticipates impending stimulus significance. Neuroimage 45:976–983

    Article  PubMed  PubMed Central  Google Scholar 

  • Marchand WR, Lee JN, Thatcher JW, Hsu EW, Rashkin E, Suchy Y, Chelune G, Starr J, Barbera SS (2008) Putamen coactivation during motor task execution. Neuroreport 19:957–960

    Article  PubMed  Google Scholar 

  • Margulies DS, Kelly AMC, Uddin LQ, Biswal BB, Castellanos FX, Milham MP (2007) Mapping the functional connectivity of anterior cingulate cortex. Neuroimage 37:579–588

    Article  PubMed  Google Scholar 

  • Menzel EW (1973) Chimpanzee spatial memory organization. Science 82:943–945

    Article  Google Scholar 

  • Mikhailova MA, Bass CE, Grinevich VP et al (2016) Optogenetically-induced tonic dopamine release from VTA-nucleus accumbens projections inhibits reward consummatory behaviors. Neuroscience 333:54–64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moga MM, Gray TS (1985) Evidence for corticotropin-releasing factor, neurotensin, and somatostatin in the neural pathway from the central nucleus of the amygdala to the parabrachial nucleus. J Comp Neurol 241:275–284

    Article  CAS  PubMed  Google Scholar 

  • Morrison SE, McGinty VB, du Hoffmann J, Nicola SM (2017) Limbic-motor integration by neural excitations and inhibitions in the nucleus accumbens. J Neurophysiol 118(5):2549–2567

    Article  PubMed  PubMed Central  Google Scholar 

  • Moscarello JM, LeDoux JE (2013) Active avoidance learning requires prefrontal suppression of amygdala-mediated defensive reactions. J Neurosci 33:3815–3823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nawa H, Takei N (2006) Recent progress in animal modeling of immune inflammatory processes in schizophrenia: implication of specific cytokines. Neurosci Res 56:2–13

    Article  CAS  PubMed  Google Scholar 

  • Nestor PJ, Graham NL, Fryer TD, Williams GB, Patterson K, Hodges JR (2003) Progressive non-fluent aphasia is associated with hypometabolism centered on the left anterior insula. Brain 126:2406–2418

    Article  Google Scholar 

  • Neumann ID, Landgraf R (2012) Balance of brain oxytocin and vasopressin: implications for anxiety, depression, and social behaviors. Trends Neurosci 35:649–659

    Article  CAS  PubMed  Google Scholar 

  • 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 96:5268–5273

    Article  CAS  PubMed  Google Scholar 

  • Oberlin BG, Dzemidzic M, Tran SM, Soeurt CM, O’Connor SJ, Yoder KY, Kareken DA (2015) Beer self-administration provokes lateralized nucleus accumbens dopamine release in male heavy drinkers. Psychopharmacology 232(5):861–870

    Article  CAS  PubMed  Google Scholar 

  • Palagi E, Cordoni G (2012) The right time to happen: play developmental divergence in the two Pan species. PLoS One 7:e52767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Paus T (2001) Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nat Rev Neurosci 2:417–424

    Article  CAS  Google Scholar 

  • Pitkänen A, Savander V, LeDoux JE (1997) Organization of intra-amygdaloid circuitries in the rat: An emerging framework for understanding functions of the amygdala. Trends Neurosci 20:517–523

    Article  PubMed  Google Scholar 

  • Pitkänen A, Kelly JL, Amaral DG (2002) Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the entorhinal cortex in the macaque monkey. Hippocampus 12:186–205

    Article  PubMed  Google Scholar 

  • Pollick AS, de Waal FBM (2007) Ape gestures and language evolution. Proc Natl Acad Sci 104:8184–8189

    Article  CAS  PubMed  Google Scholar 

  • Raghanti MA, Spurlock LB, Robert Treichler F, Weigel SE, Stimmelmayr R, Butti C, Thewissen JMGH, Hof PR (2015) An analysis of von Economo neurons in the cerebral cortex of cetaceans, artiodactyls, and perissodactyls. Brain Struct Funct 220:2303–2314

    Article  PubMed  Google Scholar 

  • Ramirez F, Moscarello JM, LeDoux JE, Sears RM (2015) Active avoidance requires a serial basal amygdala to nucleus accumbens shell circuit. J Neurosci 35:3470–3477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rilling JK, Insel TR (1999) The primate neocortex in comparative perspective using magnetic resonance imaging. J Hum Evol 37:191–223

    Article  CAS  PubMed  Google Scholar 

  • Rilling JK, Scholz J, Preuss TM, Glasser MF, Errangi BK, Behrens TE (2012) Differences between chimpanzees and bonobos in neural systems supporting social cognition. Soc Cogn Affect Neurosci 7:369–379

    Article  PubMed  Google Scholar 

  • Rizvi TA, Ennis M, Behbehani MM, Shipley MT (1991) Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: Topography and reciprocity. J Comp Neurol 303:121–131

    Article  CAS  PubMed  Google Scholar 

  • Romanski LM, LeDoux JE (1993) Information cascade from primary auditory cortex to the amygdala: corticocortical and corticoamygdaloid projections of temporal cortex in the rat. Cereb Cortex 3(6):515–532

    Article  CAS  PubMed  Google Scholar 

  • Roozendaal B, McGaugh JL (1997) Basolateral amygdala lesions block the memory-enhancing effect of glucocorticoid administration in the dorsal hippocampus of rats. Eur J Neurosci 9:76–83

    Article  CAS  PubMed  Google Scholar 

  • Rosati AG, Hare B (2012a) Chimpanzees and bonobos exhibit divergent spatial memory development. Dev Sci 15:840–853

    Article  PubMed  Google Scholar 

  • Rosati AG, Hare B (2012b) Decision making across social contexts: competition increases preferences for risk in chimpanzees and bonobos. Anim Behav 84:869–879

    Article  Google Scholar 

  • Rosati AG, Hare B (2013) Chimpanzees and bonobos exhibit emotional responses to decision outcomes. PLoS One 8(5):e63058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ross HE, Freeman SM, Spiegel LL, Ren X, Terwilliger EF, Young LJ (2009) Variation in oxytocin receptor density in the nucleus accumbens has differential effects on affiliative behaviors in monogamous and polygamous voles. J Neurosci 29:1312–1318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sah P, Faber ES, Lopez DA, Power J (2003) The amygdaloid complex: anatomy and physiology. Physiol Rev 83:803–834

    Article  CAS  PubMed  Google Scholar 

  • Santos M, Uppal N, Butti C, Wicinski B, Schmeidler J, Giannakopoulos P, Heinsen H, Schmitz C, Hof PR (2011) von Economo neurons in autism: a stereologic study of the frontoinsular cortex in children. Brain Res 1380:206–217

    Article  CAS  PubMed  Google Scholar 

  • Savonenko A, Filipkowski RK, Werka T, Zielinski K, Kaczmarek L (1999) Defensive conditioning-related functional heterogeneity among nuclei of the rat amygdala revealed by c-Fos mapping. Neurosci 94:723–733

    Article  CAS  Google Scholar 

  • Saygin ZM, Osher DE, Augustinack J, Fischl B, Gabrieli JDE (2011) Connectivity-based segmentation of human amygdala nuclei using probabilistic tractography. Neuroimage 56:1353–1361

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Schenker NM, Buxhoeveden DP, Blackmon WL, Amunts K, Zilles K, Semendeferi K (2008) A comparative quantitative analysis of cytoarchitecture and minicolumnar organization in Broca’s area in humans and great apes. J Comp Neurol 510:117–128

    Article  PubMed  Google Scholar 

  • Seeley WW (2010) Anterior insula degeneration in frontotemporal dementia. Brain Struct Funct 5–6:465–475

    Article  Google Scholar 

  • Senatorov VV, Damadzic R, Mann CL, Schwandt ML, George DT, Hommer DW, Heilig M, Momenan R (2014) Reduced anterior insula, enlarged amygdala in alcoholism and associated depleted von Economo neurons. Brain 138:69–79

    Article  PubMed  PubMed Central  Google Scholar 

  • Simmons AN, Stein MB, Strigo IA, Arce E, Hitchcock C, Paulus MP (2011) Anxiety positive subjects show altered processing in the anterior insula during anticipation of negative stimuli. Hum Brain Mapp 32:1836–1846

    Article  PubMed  Google Scholar 

  • Singleton I, Van Schaik CP (2002) The social organization of a population of Sumatran orang-utans. Folia Primatol 73:1–20

    Article  PubMed  Google Scholar 

  • Spocter MA, Hopkins WD, Barks SK, Bianchi S, Hehmeyer AE, Anderson SM, Stimpson CD, Fobbs AJ, Hof PR, Sherwood CC (2012) Neuropil distribution in the cerebral cortex differs between humans and chimpanzees. J Comp Neurol 520:2917–2929

    Article  PubMed  PubMed Central  Google Scholar 

  • Staes N, Stevens JMG, Helsen P, Hillyer M, Korody M, Eens M (2014) Oxytocin and vasopressin receptor gene variation as a proximate base for inter- and intraspecific behavioral differences in bonobos and chimpanzees. PLoS One 9:1–9

    Article  CAS  Google Scholar 

  • Staes N, Koski SE, Helsen P, Fransen E, Eens M, Stevens JMG (2015) Chimpanzee sociability is associated with vasopressin (Avpr1a) but not oxytocin receptor gene (OXTR) variation. Horm Behavior 75:84–90

    Article  CAS  Google Scholar 

  • Staes N, Weiss A, Helsen P, Korody M, Eens M, Stevens JMG (2016) Bonobo personality traits are heritable and associated with vasopressin receptor gene 1a variation. Sci Rep 6(1):38193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stevens JMG, Vervaecke H, De Vries H, Van Elsacker L (2007) Sex differences in the steepness of dominance hierarchies in captive bonobo groups. Int J Primatol 28:1417–1430

    Article  Google Scholar 

  • Stimpson CD, Tetreault NA, Allman JM, Jacobs B, Butti C, Hof PR, Sherwood CC (2011) Biochemical specificity of Von Economo neurons in hominoids. Am J Hum Biol 23:22–28

    Article  PubMed  PubMed Central  Google Scholar 

  • Stimpson CD, Barger N, Taglialatela JP, Gendron-Fitzpatrick A, Hof PR, Hopkins WD, Sherwood CC (2015) Differential serotonergic innervation of the amygdala in bonobos and chimpanzees. Soc Cogn Affect Neurosci 11:413–422

    Article  PubMed  PubMed Central  Google Scholar 

  • Tan J, Hare B (2013) Bonobos share with strangers. PLoS One 8(1):e51922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turner BH, Herkenham M (1991) Thalamoamygdaloid projections in the rat: a test of the amygdala’s role in sensory processing. J Comp Neurol 313:295–325

    Article  CAS  PubMed  Google Scholar 

  • Van Schaik CP (1999) The socioecology of fission-fusion sociality in orangutans. Primates 40:69–86

    Article  PubMed  Google Scholar 

  • Veening JG, Swanson LW, Sawchenko PE (1984) The organization of projections from the central nucleus of the amygdala to brainstem sites involved in central autonomic regulation: a combined retrograde transport-immunohistochemical study. Brain Res 303:337–357

    Article  CAS  PubMed  Google Scholar 

  • Vervaecke H, De Vries H, Van Elsacker L (2000) Dominance and its behavioral measures in a captive group of bonobos (Pan paniscus). Int J Primatol 21:47–68

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Whalen PJ, Rauch SL, Etcoff NL, McInerney SC, Lee MB, Jenike MA (1998) Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J Neurosci 18:411–418

    Article  CAS  PubMed  Google Scholar 

  • Wich SA, Utami-Atmoko SS, Mitra Setia T, Rijksen HD, Schürmann C, van Hoof JARAM, van Schaik CP (2004) Life history of wild sumatran orangutans (Pongo abelii). J Hum Evol 47:385–398

    Article  CAS  PubMed  Google Scholar 

  • Wilson ML, Boesch C, Fruth B et al (2014) Lethal aggression in Pan is better explained by adaptive strategies than human impacts. Nature 513:414–417

    Article  CAS  PubMed  Google Scholar 

  • Wittling W, Block A, Schweiger E, Genzel S (1998) Hemisphere asymmetry in sympathetic control of the human myocardium. Brain Cogn 38:17–35

    Article  CAS  PubMed  Google Scholar 

  • Wobber V, Hare B, Lipson S, Wrangham R, Ellison P (2013) Different ontogenetic patterns of testosterone production reflect divergent male reproductive strategies in chimpanzees and bonobos. Physiol Behav 116–117:44–53

    Article  CAS  PubMed  Google Scholar 

  • Woods V, Hare B (2011) Bonobo but not chimpanzee infants use socio-sexual contact with peers. Primates 52:111–116

    Article  PubMed  Google Scholar 

  • Wrangham RW (1993) The evolution of sexuality in chimpanzees and bonobos. Hum Nat 4:47–79

    Article  CAS  PubMed  Google Scholar 

  • Wree A, Schleicher A, Zilles K (1982) Estimation of volume fractions in nervous tissue with an image analyzer. J Neurosci Methods 6:29–43

    Article  CAS  PubMed  Google Scholar 

  • Yu K, Garcia da Silva P, Albeanu DF, Li B (2016) Central amygdala somatostatin neurons gate passive and active defensive behaviors. J Neurosci 36:6488–6496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors would like to thank Yerkes National Primate Research Center (supported by National Institutes for Health Grant ORIP/OD P51 OD011132), the National Chimpanzee Brain Resource (supported by National Institutes for Health Grant R24 NS092988-02), Milwaukee County Zoo, Jacksonville Zoo, and veterinary technicians for the donation of specimens. We would also like to thank Dr. Amy Bauernfeind for helpful discussion and Dr. John Allman for providing bonobo samples. This work was supported by the National Science Foundation (SMA-1542848) and the James S. McDonnell Foundation (220020293).

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Authors and Affiliations

  1. Department of Anthropology, Center for the Advanced Study of Human Paleobiology, The George Washington University, Washington, DC, 20052, USA

    Habon A. Issa, Nicky Staes, Sophia Diggs-Galligan, Cheryl D. Stimpson & Chet C. Sherwood

  2. Comparative Pathology Lab-RARC, University of Wisconsin, Madison, WI, 53726, USA

    Annette Gendron-Fitzpatrick

  3. Department of Ecology, Evolution, and Organismal Biology, Kennesaw State University, Kennesaw, GA, 30144, USA

    Jared P. Taglialatela

  4. Ape Cognition and Conservation Initiative, Des Moines, IA, 50320, USA

    Jared P. Taglialatela & William D. Hopkins

  5. Fishberg Department of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA

    Patrick R. Hof

  6. Neuroscience Institute and Language Research Center, Georgia State University, Atlanta, GA, 30322, USA

    William D. Hopkins

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  1. Habon A. Issa
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Correspondence to Habon A. Issa.

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Issa, H.A., Staes, N., Diggs-Galligan, S. et al. Comparison of bonobo and chimpanzee brain microstructure reveals differences in socio-emotional circuits. Brain Struct Funct 224, 239–251 (2019). https://doi.org/10.1007/s00429-018-1751-9

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