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Erschienen in: Brain Structure and Function 1/2019

10.10.2018 | Original Article

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

verfasst von: Habon A. Issa, Nicky Staes, Sophia Diggs-Galligan, Cheryl D. Stimpson, Annette Gendron-Fitzpatrick, Jared P. Taglialatela, Patrick R. Hof, William D. Hopkins, Chet C. Sherwood

Erschienen in: Brain Structure and Function | Ausgabe 1/2019

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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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Literatur
Zurück zum Zitat 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 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
Zurück zum Zitat 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 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
Zurück zum Zitat 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 4:147CrossRefPubMedPubMedCentral 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 4:147CrossRefPubMedPubMedCentral
Zurück zum Zitat Allman JM, Hakeem A, Erwin JM, Nimchinsky E, Hof PR (2001) The anterior cingulate cortex. Ann N Y Acad Sci 935:107–117CrossRefPubMed Allman JM, Hakeem A, Erwin JM, Nimchinsky E, Hof PR (2001) The anterior cingulate cortex. Ann N Y Acad Sci 935:107–117CrossRefPubMed
Zurück zum Zitat Allman JM, Watson KK, Tetreault NA, Hakeem AY (2005) Intuition and autism: a possible role for von Economo neurons. Trends Cogn Sci 9:367–373CrossRefPubMed Allman JM, Watson KK, Tetreault NA, Hakeem AY (2005) Intuition and autism: a possible role for von Economo neurons. Trends Cogn Sci 9:367–373CrossRefPubMed
Zurück zum Zitat 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 214:495–517CrossRefPubMed 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 214:495–517CrossRefPubMed
Zurück zum Zitat Amaral DG, Price JL (1984) Amygdalo-cortical projections in the monkey (Macaca fascicularis). J Comp Neurol 230:465–496CrossRefPubMed Amaral DG, Price JL (1984) Amygdalo-cortical projections in the monkey (Macaca fascicularis). J Comp Neurol 230:465–496CrossRefPubMed
Zurück zum Zitat Bales KL, Carter CS (2003) Sex differences and developmental effects of oxytocin on aggression and social behavior in prairie voles (Microtus ochrogaster). Horm Behav 44:178–184CrossRefPubMed Bales KL, Carter CS (2003) Sex differences and developmental effects of oxytocin on aggression and social behavior in prairie voles (Microtus ochrogaster). Horm Behav 44:178–184CrossRefPubMed
Zurück zum Zitat 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 134:392–403CrossRefPubMed 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 134:392–403CrossRefPubMed
Zurück zum Zitat 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 99:11435–11440CrossRefPubMed 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 99:11435–11440CrossRefPubMed
Zurück zum Zitat 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 64:263–279CrossRefPubMedPubMedCentral 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 64:263–279CrossRefPubMedPubMedCentral
Zurück zum Zitat 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 66:83–88CrossRefPubMed 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 66:83–88CrossRefPubMed
Zurück zum Zitat 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 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
Zurück zum Zitat 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 61:293–303CrossRefPubMed 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 61:293–303CrossRefPubMed
Zurück zum Zitat 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 119:771–778CrossRefPubMed 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 119:771–778CrossRefPubMed
Zurück zum Zitat 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 661:11–17CrossRefPubMed 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 661:11–17CrossRefPubMed
Zurück zum Zitat 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 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
Zurück zum Zitat Butti C, Santos M, Uppal N, Hof PR (2013) Von economo neurons: clinical and evolutionary perspectives. Cortex 49(1):312–326CrossRefPubMed Butti C, Santos M, Uppal N, Hof PR (2013) Von economo neurons: clinical and evolutionary perspectives. Cortex 49(1):312–326CrossRefPubMed
Zurück zum Zitat 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):670–700CrossRef 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):670–700CrossRef
Zurück zum Zitat Campbell A (2008) Attachment, aggression and affiliation: the role of oxytocin in female social behavior. Biol Psychol 77:1–10CrossRefPubMed Campbell A (2008) Attachment, aggression and affiliation: the role of oxytocin in female social behavior. Biol Psychol 77:1–10CrossRefPubMed
Zurück zum Zitat 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 22:247–257CrossRefPubMedPubMedCentral 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 22:247–257CrossRefPubMedPubMedCentral
Zurück zum Zitat Casanova MF, Buxhoeveden DP, Switala AE, Roy E (2002) Minicolumnar pathology in autism. Neurology 58:428–432CrossRefPubMed Casanova MF, Buxhoeveden DP, Switala AE, Roy E (2002) Minicolumnar pathology in autism. Neurology 58:428–432CrossRefPubMed
Zurück zum Zitat Casanova MF, van Kooten IAJ, Switala AE et al (2006) Minicolumnar abnormalities in autism. Acta Neuropathol 112:287–303CrossRefPubMed Casanova MF, van Kooten IAJ, Switala AE et al (2006) Minicolumnar abnormalities in autism. Acta Neuropathol 112:287–303CrossRefPubMed
Zurück zum Zitat Cobos I, Seeley WW (2013) Human von Economo neurons express transcription factors associated with layer V subcerebral projection neurons. Cereb Cortex 25:213–220CrossRefPubMedPubMedCentral Cobos I, Seeley WW (2013) Human von Economo neurons express transcription factors associated with layer V subcerebral projection neurons. Cereb Cortex 25:213–220CrossRefPubMedPubMedCentral
Zurück zum Zitat 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 33:165–179CrossRefPubMed 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 33:165–179CrossRefPubMed
Zurück zum Zitat 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 15:225–230CrossRefPubMed 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 15:225–230CrossRefPubMed
Zurück zum Zitat Craig AD (2005) Forebrain emotional asymmetry: a neuroanatomical basis? Trends Cogn Sci 9:566–571CrossRefPubMed Craig AD (2005) Forebrain emotional asymmetry: a neuroanatomical basis? Trends Cogn Sci 9:566–571CrossRefPubMed
Zurück zum Zitat Dajani DR, Uddin LQ (2016) Local brain connectivity across development in autism spectrum disorder: a cross-sectional investigation. Autism Res 9:43–54CrossRefPubMed Dajani DR, Uddin LQ (2016) Local brain connectivity across development in autism spectrum disorder: a cross-sectional investigation. Autism Res 9:43–54CrossRefPubMed
Zurück zum Zitat De Waal FM (1988) The communicative repertoire of captive bonobos (Pan paniscus), compared to that of chimpanzees. Behav 106:183–251CrossRef De Waal FM (1988) The communicative repertoire of captive bonobos (Pan paniscus), compared to that of chimpanzees. Behav 106:183–251CrossRef
Zurück zum Zitat Delgado RA, Van Schaik CP (2000) The behavioral ecology and conservation of the orangutan (Pongo pygmaeus): a tale of two islands. Evol Anthropol 9:201–218CrossRef Delgado RA, Van Schaik CP (2000) The behavioral ecology and conservation of the orangutan (Pongo pygmaeus): a tale of two islands. Evol Anthropol 9:201–218CrossRef
Zurück zum Zitat Devinsky O, Morrell MJ, Vogt BA (1995) Contributions of anterior cingulate cortex to behaviour. Brain 118:279–306CrossRefPubMed Devinsky O, Morrell MJ, Vogt BA (1995) Contributions of anterior cingulate cortex to behaviour. Brain 118:279–306CrossRefPubMed
Zurück zum Zitat 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 28:131–144CrossRef 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 28:131–144CrossRef
Zurück zum Zitat 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 8:180CrossRefPubMedPubMedCentral 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 8:180CrossRefPubMedPubMedCentral
Zurück zum Zitat Duerden EG, Arsalidou M, Lee M, Taylor MJ (2013) Lateralization of affective processing in the insula. NeuroImage 78:159–175CrossRefPubMed Duerden EG, Arsalidou M, Lee M, Taylor MJ (2013) Lateralization of affective processing in the insula. NeuroImage 78:159–175CrossRefPubMed
Zurück zum Zitat Etkin A, Egner T, Kalisch R (2011) Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn Sci 15:85–93CrossRefPubMed Etkin A, Egner T, Kalisch R (2011) Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn Sci 15:85–93CrossRefPubMed
Zurück zum Zitat Evrard HC, Forro T, Logothetis NK (2012) Von Economo neurons in the anterior insula of the macaque monkey. Neuron 74:482–489CrossRef Evrard HC, Forro T, Logothetis NK (2012) Von Economo neurons in the anterior insula of the macaque monkey. Neuron 74:482–489CrossRef
Zurück zum Zitat Fadok JP, Markovic M, Tovote P, Lüthi A (2018) New perspectives on central amygdala function. Curr Opin Neurobiol 49:141–147CrossRefPubMed Fadok JP, Markovic M, Tovote P, Lüthi A (2018) New perspectives on central amygdala function. Curr Opin Neurobiol 49:141–147CrossRefPubMed
Zurück zum Zitat Floresco SB (2015) The nucleus accumbens: an interface between cognition, emotion, and action. Annu Rev Psychol 66:25–52CrossRefPubMed Floresco SB (2015) The nucleus accumbens: an interface between cognition, emotion, and action. Annu Rev Psychol 66:25–52CrossRefPubMed
Zurück zum Zitat 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):345–365CrossRefPubMed 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):345–365CrossRefPubMed
Zurück zum Zitat Furuichi T (1997) Agonistic interactions and matrifocal dominance rank of wild bonobos (pan paniscus) at wamba. Int J Primatol 18:855–875CrossRef Furuichi T (1997) Agonistic interactions and matrifocal dominance rank of wild bonobos (pan paniscus) at wamba. Int J Primatol 18:855–875CrossRef
Zurück zum Zitat Furuichi T (2011) Female contributions to the peaceful nature of bonobo society. Evol Anthropol 20:131–142CrossRefPubMed Furuichi T (2011) Female contributions to the peaceful nature of bonobo society. Evol Anthropol 20:131–142CrossRefPubMed
Zurück zum Zitat Galdikas BMF (1985) Orangutan sociality at Tanjung Puting. Am J Primatol 9:101–119CrossRef Galdikas BMF (1985) Orangutan sociality at Tanjung Puting. Am J Primatol 9:101–119CrossRef
Zurück zum Zitat Goodall J (1986) The Chimpanzees of Gombe: patterns of behavior. Harvard University Press, Cambridge Goodall J (1986) The Chimpanzees of Gombe: patterns of behavior. Harvard University Press, Cambridge
Zurück zum Zitat Gray JR, Braver TS (2002) Personality predicts working-memory-related activation in the caudal anterior cingulate cortex. Cogn Affect Behav Neurosci 2:64–75CrossRefPubMed Gray JR, Braver TS (2002) Personality predicts working-memory-related activation in the caudal anterior cingulate cortex. Cogn Affect Behav Neurosci 2:64–75CrossRefPubMed
Zurück zum Zitat Graziano M (2005) Arm movements evoked by electrical stimulation in the motor cortex of monkeys. J Neurophysiol 94:4209–4223CrossRefPubMed Graziano M (2005) Arm movements evoked by electrical stimulation in the motor cortex of monkeys. J Neurophysiol 94:4209–4223CrossRefPubMed
Zurück zum Zitat Groenewegen HJ, Wright CI, Beijer AV (1996) The nucleus accumbens: gateway for limbic structures to reach the motor system? Prog Brain Res 107:485–511CrossRefPubMed Groenewegen HJ, Wright CI, Beijer AV (1996) The nucleus accumbens: gateway for limbic structures to reach the motor system? Prog Brain Res 107:485–511CrossRefPubMed
Zurück zum Zitat Gruber T, Clay Z (2016) A comparison between bonobos and chimpanzees: a review and update. Evol Anthropol 25:239–252CrossRefPubMed Gruber T, Clay Z (2016) A comparison between bonobos and chimpanzees: a review and update. Evol Anthropol 25:239–252CrossRefPubMed
Zurück zum Zitat 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):1023–1033CrossRef 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):1023–1033CrossRef
Zurück zum Zitat Gundersen HJG, Jensen EBV, Kieu K et al (1999) The efficiency of systematic sampling in stereology—reconsidered. J Microsc 193:199–211CrossRefPubMed Gundersen HJG, Jensen EBV, Kieu K et al (1999) The efficiency of systematic sampling in stereology—reconsidered. J Microsc 193:199–211CrossRefPubMed
Zurück zum Zitat 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 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
Zurück zum Zitat 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.e18CrossRefPubMedPubMedCentral 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.e18CrossRefPubMedPubMedCentral
Zurück zum Zitat Hare B, Melis AP, Woods V, Hastings S, Wrangham R (2007) Tolerance allows bonobos to outperform chimpanzees on a cooperative task. Curr Biol 17:619–623CrossRefPubMed Hare B, Melis AP, Woods V, Hastings S, Wrangham R (2007) Tolerance allows bonobos to outperform chimpanzees on a cooperative task. Curr Biol 17:619–623CrossRefPubMed
Zurück zum Zitat Herrmann E, Hare B, Call J, Tomasello M (2010) Differences in the cognitive skills of bonobos and chimpanzees. PLoS One 5:2–5 Herrmann E, Hare B, Call J, Tomasello M (2010) Differences in the cognitive skills of bonobos and chimpanzees. PLoS One 5:2–5
Zurück zum Zitat Herrmann E, Hare B, Cissewski J, Tomasello M (2011) A comparison of temperament in nonhuman apes and human infants. Dev Sci 14:1393–1405CrossRefPubMed Herrmann E, Hare B, Cissewski J, Tomasello M (2011) A comparison of temperament in nonhuman apes and human infants. Dev Sci 14:1393–1405CrossRefPubMed
Zurück zum Zitat 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 142:23–35CrossRefPubMed 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 142:23–35CrossRefPubMed
Zurück zum Zitat 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, Van Der Gucht E (2007) Structure of the cerebral cortex of the humpback whale, Megaptera novaeangliae (Cetacea, Mysticeti, Balaenopteridae). Anat Rec 290:1–31CrossRef
Zurück zum Zitat Holdefer RN, Miller LE (2002) Primary motor cortical neurons encode functional muscle synergies. Exp Brain Res 146:233–243CrossRefPubMed Holdefer RN, Miller LE (2002) Primary motor cortical neurons encode functional muscle synergies. Exp Brain Res 146:233–243CrossRefPubMed
Zurück zum Zitat 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 7:497–498CrossRefPubMed 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 7:497–498CrossRefPubMed
Zurück zum Zitat 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 71:988–997CrossRefPubMedPubMedCentral 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 71:988–997CrossRefPubMedPubMedCentral
Zurück zum Zitat 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 11:552–558CrossRefPubMedPubMedCentral 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 11:552–558CrossRefPubMedPubMedCentral
Zurück zum Zitat 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 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
Zurück zum Zitat Hrybouski S, Aghamohammadi-Sereshki A, Madan CR et al (2016) Amygdala subnuclei response and connectivity during emotional processing. Neuroimage 133:98–110CrossRefPubMed Hrybouski S, Aghamohammadi-Sereshki A, Madan CR et al (2016) Amygdala subnuclei response and connectivity during emotional processing. Neuroimage 133:98–110CrossRefPubMed
Zurück zum Zitat 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 28:6950–6959CrossRefPubMedPubMedCentral 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 28:6950–6959CrossRefPubMedPubMedCentral
Zurück zum Zitat 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 24:5506–5515CrossRefPubMed 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 24:5506–5515CrossRefPubMed
Zurück zum Zitat 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 116:479–489CrossRefPubMed 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 116:479–489CrossRefPubMed
Zurück zum Zitat 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 9:47CrossRefPubMedPubMedCentral 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 9:47CrossRefPubMedPubMedCentral
Zurück zum Zitat Keverne EB, Curley JP (2004) Vasopressin, oxytocin and social behaviour. Curr Opin Neurobiol 14:777–783CrossRefPubMed Keverne EB, Curley JP (2004) Vasopressin, oxytocin and social behaviour. Curr Opin Neurobiol 14:777–783CrossRefPubMed
Zurück zum Zitat 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 22:251–259CrossRefPubMedPubMedCentral 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 22:251–259CrossRefPubMedPubMedCentral
Zurück zum Zitat 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 89:273–276CrossRefPubMed 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 89:273–276CrossRefPubMed
Zurück zum Zitat Knutson B, Adams CM, Fong GW, Hommer D (2001) Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J Neurosci 21:RC159CrossRefPubMed Knutson B, Adams CM, Fong GW, Hommer D (2001) Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J Neurosci 21:RC159CrossRefPubMed
Zurück zum Zitat 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 133:55–65CrossRefPubMed 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 133:55–65CrossRefPubMed
Zurück zum Zitat 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 67:1120–1127CrossRefPubMedPubMedCentral 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 67:1120–1127CrossRefPubMedPubMedCentral
Zurück zum Zitat 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 8:2517–2529CrossRefPubMed 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 8:2517–2529CrossRefPubMed
Zurück zum Zitat 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):1062–1069CrossRefPubMed 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):1062–1069CrossRefPubMed
Zurück zum Zitat Liu Y, Wang ZX (2003) Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles. Neurosci 121:537–544CrossRef Liu Y, Wang ZX (2003) Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles. Neurosci 121:537–544CrossRef
Zurück zum Zitat Lorberbaum JP, Newman JD, Horwitz AR et al (2002) A potential role for thalamocingulate circuitry in human maternal behavior. Biol Psychiatry 51:431–445CrossRefPubMed Lorberbaum JP, Newman JD, Horwitz AR et al (2002) A potential role for thalamocingulate circuitry in human maternal behavior. Biol Psychiatry 51:431–445CrossRefPubMed
Zurück zum Zitat 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 19:957–960CrossRefPubMed 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 19:957–960CrossRefPubMed
Zurück zum Zitat Margulies DS, Kelly AMC, Uddin LQ, Biswal BB, Castellanos FX, Milham MP (2007) Mapping the functional connectivity of anterior cingulate cortex. Neuroimage 37:579–588CrossRefPubMed Margulies DS, Kelly AMC, Uddin LQ, Biswal BB, Castellanos FX, Milham MP (2007) Mapping the functional connectivity of anterior cingulate cortex. Neuroimage 37:579–588CrossRefPubMed
Zurück zum Zitat Menzel EW (1973) Chimpanzee spatial memory organization. Science 82:943–945CrossRef Menzel EW (1973) Chimpanzee spatial memory organization. Science 82:943–945CrossRef
Zurück zum Zitat Mikhailova MA, Bass CE, Grinevich VP et al (2016) Optogenetically-induced tonic dopamine release from VTA-nucleus accumbens projections inhibits reward consummatory behaviors. Neuroscience 333:54–64CrossRefPubMedPubMedCentral Mikhailova MA, Bass CE, Grinevich VP et al (2016) Optogenetically-induced tonic dopamine release from VTA-nucleus accumbens projections inhibits reward consummatory behaviors. Neuroscience 333:54–64CrossRefPubMedPubMedCentral
Zurück zum Zitat 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 241:275–284CrossRefPubMed 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 241:275–284CrossRefPubMed
Zurück zum Zitat 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):2549–2567CrossRefPubMedPubMedCentral 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):2549–2567CrossRefPubMedPubMedCentral
Zurück zum Zitat Moscarello JM, LeDoux JE (2013) Active avoidance learning requires prefrontal suppression of amygdala-mediated defensive reactions. J Neurosci 33:3815–3823CrossRefPubMedPubMedCentral Moscarello JM, LeDoux JE (2013) Active avoidance learning requires prefrontal suppression of amygdala-mediated defensive reactions. J Neurosci 33:3815–3823CrossRefPubMedPubMedCentral
Zurück zum Zitat Nawa H, Takei N (2006) Recent progress in animal modeling of immune inflammatory processes in schizophrenia: implication of specific cytokines. Neurosci Res 56:2–13CrossRefPubMed Nawa H, Takei N (2006) Recent progress in animal modeling of immune inflammatory processes in schizophrenia: implication of specific cytokines. Neurosci Res 56:2–13CrossRefPubMed
Zurück zum Zitat 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 126:2406–2418CrossRef 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 126:2406–2418CrossRef
Zurück zum Zitat Neumann ID, Landgraf R (2012) Balance of brain oxytocin and vasopressin: implications for anxiety, depression, and social behaviors. Trends Neurosci 35:649–659CrossRefPubMed Neumann ID, Landgraf R (2012) Balance of brain oxytocin and vasopressin: implications for anxiety, depression, and social behaviors. Trends Neurosci 35:649–659CrossRefPubMed
Zurück zum Zitat 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 96:5268–5273CrossRefPubMed 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 96:5268–5273CrossRefPubMed
Zurück zum Zitat 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):861–870CrossRefPubMed 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):861–870CrossRefPubMed
Zurück zum Zitat Paus T (2001) Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nat Rev Neurosci 2:417–424CrossRef Paus T (2001) Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nat Rev Neurosci 2:417–424CrossRef
Zurück zum Zitat 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 20:517–523CrossRefPubMed 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 20:517–523CrossRefPubMed
Zurück zum Zitat 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 12:186–205CrossRefPubMed 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 12:186–205CrossRefPubMed
Zurück zum Zitat Pollick AS, de Waal FBM (2007) Ape gestures and language evolution. Proc Natl Acad Sci 104:8184–8189CrossRefPubMed Pollick AS, de Waal FBM (2007) Ape gestures and language evolution. Proc Natl Acad Sci 104:8184–8189CrossRefPubMed
Zurück zum Zitat 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 220:2303–2314CrossRefPubMed 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 220:2303–2314CrossRefPubMed
Zurück zum Zitat Ramirez F, Moscarello JM, LeDoux JE, Sears RM (2015) Active avoidance requires a serial basal amygdala to nucleus accumbens shell circuit. J Neurosci 35:3470–3477CrossRefPubMedPubMedCentral Ramirez F, Moscarello JM, LeDoux JE, Sears RM (2015) Active avoidance requires a serial basal amygdala to nucleus accumbens shell circuit. J Neurosci 35:3470–3477CrossRefPubMedPubMedCentral
Zurück zum Zitat Rilling JK, Insel TR (1999) The primate neocortex in comparative perspective using magnetic resonance imaging. J Hum Evol 37:191–223CrossRefPubMed Rilling JK, Insel TR (1999) The primate neocortex in comparative perspective using magnetic resonance imaging. J Hum Evol 37:191–223CrossRefPubMed
Zurück zum Zitat 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 7:369–379CrossRefPubMed 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 7:369–379CrossRefPubMed
Zurück zum Zitat 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 303:121–131CrossRefPubMed 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 303:121–131CrossRefPubMed
Zurück zum Zitat 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):515–532CrossRefPubMed 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):515–532CrossRefPubMed
Zurück zum Zitat 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 9:76–83CrossRefPubMed 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 9:76–83CrossRefPubMed
Zurück zum Zitat Rosati AG, Hare B (2012a) Chimpanzees and bonobos exhibit divergent spatial memory development. Dev Sci 15:840–853CrossRefPubMed Rosati AG, Hare B (2012a) Chimpanzees and bonobos exhibit divergent spatial memory development. Dev Sci 15:840–853CrossRefPubMed
Zurück zum Zitat Rosati AG, Hare B (2012b) Decision making across social contexts: competition increases preferences for risk in chimpanzees and bonobos. Anim Behav 84:869–879CrossRef Rosati AG, Hare B (2012b) Decision making across social contexts: competition increases preferences for risk in chimpanzees and bonobos. Anim Behav 84:869–879CrossRef
Zurück zum Zitat 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 29:1312–1318CrossRefPubMedPubMedCentral 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 29:1312–1318CrossRefPubMedPubMedCentral
Zurück zum Zitat Sah P, Faber ES, Lopez DA, Power J (2003) The amygdaloid complex: anatomy and physiology. Physiol Rev 83:803–834CrossRefPubMed Sah P, Faber ES, Lopez DA, Power J (2003) The amygdaloid complex: anatomy and physiology. Physiol Rev 83:803–834CrossRefPubMed
Zurück zum Zitat 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 1380:206–217CrossRefPubMed 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 1380:206–217CrossRefPubMed
Zurück zum Zitat 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 94:723–733CrossRef 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 94:723–733CrossRef
Zurück zum Zitat Saygin ZM, Osher DE, Augustinack J, Fischl B, Gabrieli JDE (2011) Connectivity-based segmentation of human amygdala nuclei using probabilistic tractography. Neuroimage 56:1353–1361CrossRefPubMedPubMedCentral Saygin ZM, Osher DE, Augustinack J, Fischl B, Gabrieli JDE (2011) Connectivity-based segmentation of human amygdala nuclei using probabilistic tractography. Neuroimage 56:1353–1361CrossRefPubMedPubMedCentral
Zurück zum Zitat Schenker NM, Desgouttes AM, Semendeferi K (2005) Neural connectivity and cortical substrates of cognition in hominoids. J Hum Evol 49:547–569CrossRefPubMed Schenker NM, Desgouttes AM, Semendeferi K (2005) Neural connectivity and cortical substrates of cognition in hominoids. J Hum Evol 49:547–569CrossRefPubMed
Zurück zum Zitat 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 510:117–128CrossRefPubMed 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 510:117–128CrossRefPubMed
Zurück zum Zitat Seeley WW (2010) Anterior insula degeneration in frontotemporal dementia. Brain Struct Funct 5–6:465–475CrossRef Seeley WW (2010) Anterior insula degeneration in frontotemporal dementia. Brain Struct Funct 5–6:465–475CrossRef
Zurück zum Zitat 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 138:69–79CrossRefPubMedPubMedCentral 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 138:69–79CrossRefPubMedPubMedCentral
Zurück zum Zitat 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 32:1836–1846CrossRefPubMed 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 32:1836–1846CrossRefPubMed
Zurück zum Zitat Singleton I, Van Schaik CP (2002) The social organization of a population of Sumatran orang-utans. Folia Primatol 73:1–20CrossRefPubMed Singleton I, Van Schaik CP (2002) The social organization of a population of Sumatran orang-utans. Folia Primatol 73:1–20CrossRefPubMed
Zurück zum Zitat 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 520:2917–2929CrossRefPubMedPubMedCentral 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 520:2917–2929CrossRefPubMedPubMedCentral
Zurück zum Zitat 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 9:1–9CrossRef 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 9:1–9CrossRef
Zurück zum Zitat 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 75:84–90CrossRef 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 75:84–90CrossRef
Zurück zum Zitat 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):38193CrossRefPubMedPubMedCentral 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):38193CrossRefPubMedPubMedCentral
Zurück zum Zitat 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 28:1417–1430CrossRef 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 28:1417–1430CrossRef
Zurück zum Zitat 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 23:22–28CrossRefPubMedPubMedCentral 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 23:22–28CrossRefPubMedPubMedCentral
Zurück zum Zitat 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 11:413–422CrossRefPubMedPubMedCentral 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 11:413–422CrossRefPubMedPubMedCentral
Zurück zum Zitat Turner BH, Herkenham M (1991) Thalamoamygdaloid projections in the rat: a test of the amygdala’s role in sensory processing. J Comp Neurol 313:295–325CrossRefPubMed Turner BH, Herkenham M (1991) Thalamoamygdaloid projections in the rat: a test of the amygdala’s role in sensory processing. J Comp Neurol 313:295–325CrossRefPubMed
Zurück zum Zitat Van Schaik CP (1999) The socioecology of fission-fusion sociality in orangutans. Primates 40:69–86CrossRefPubMed Van Schaik CP (1999) The socioecology of fission-fusion sociality in orangutans. Primates 40:69–86CrossRefPubMed
Zurück zum Zitat 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 303:337–357CrossRefPubMed 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 303:337–357CrossRefPubMed
Zurück zum Zitat 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 21:47–68CrossRef 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 21:47–68CrossRef
Zurück zum Zitat Watson KK, Jones TK, Allman JM (2006) Dendritic architecture of the von economo neurons. Neurosci 141:1107–1112CrossRef Watson KK, Jones TK, Allman JM (2006) Dendritic architecture of the von economo neurons. Neurosci 141:1107–1112CrossRef
Zurück zum Zitat 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 18:411–418CrossRefPubMed 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 18:411–418CrossRefPubMed
Zurück zum Zitat 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 47:385–398CrossRefPubMed 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 47:385–398CrossRefPubMed
Zurück zum Zitat Wilson ML, Boesch C, Fruth B et al (2014) Lethal aggression in Pan is better explained by adaptive strategies than human impacts. Nature 513:414–417CrossRefPubMed Wilson ML, Boesch C, Fruth B et al (2014) Lethal aggression in Pan is better explained by adaptive strategies than human impacts. Nature 513:414–417CrossRefPubMed
Zurück zum Zitat Wittling W, Block A, Schweiger E, Genzel S (1998) Hemisphere asymmetry in sympathetic control of the human myocardium. Brain Cogn 38:17–35CrossRefPubMed Wittling W, Block A, Schweiger E, Genzel S (1998) Hemisphere asymmetry in sympathetic control of the human myocardium. Brain Cogn 38:17–35CrossRefPubMed
Zurück zum Zitat 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 116–117:44–53CrossRefPubMed 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 116–117:44–53CrossRefPubMed
Zurück zum Zitat Woods V, Hare B (2011) Bonobo but not chimpanzee infants use socio-sexual contact with peers. Primates 52:111–116CrossRefPubMed Woods V, Hare B (2011) Bonobo but not chimpanzee infants use socio-sexual contact with peers. Primates 52:111–116CrossRefPubMed
Zurück zum Zitat Wree A, Schleicher A, Zilles K (1982) Estimation of volume fractions in nervous tissue with an image analyzer. J Neurosci Methods 6:29–43CrossRefPubMed Wree A, Schleicher A, Zilles K (1982) Estimation of volume fractions in nervous tissue with an image analyzer. J Neurosci Methods 6:29–43CrossRefPubMed
Zurück zum Zitat Yu K, Garcia da Silva P, Albeanu DF, Li B (2016) Central amygdala somatostatin neurons gate passive and active defensive behaviors. J Neurosci 36:6488–6496CrossRefPubMedPubMedCentral Yu K, Garcia da Silva P, Albeanu DF, Li B (2016) Central amygdala somatostatin neurons gate passive and active defensive behaviors. J Neurosci 36:6488–6496CrossRefPubMedPubMedCentral
Metadaten
Titel
Comparison of bonobo and chimpanzee brain microstructure reveals differences in socio-emotional circuits
verfasst von
Habon A. Issa
Nicky Staes
Sophia Diggs-Galligan
Cheryl D. Stimpson
Annette Gendron-Fitzpatrick
Jared P. Taglialatela
Patrick R. Hof
William D. Hopkins
Chet C. Sherwood
Publikationsdatum
10.10.2018
Verlag
Springer Berlin Heidelberg
Erschienen in
Brain Structure and Function / Ausgabe 1/2019
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-018-1751-9

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