Skip to main content
main-content
Erschienen in: Brain Structure and Function 6/2021

25.05.2021 | Original Article

The nucleus accumbens and ventral pallidum exhibit greater dopaminergic innervation in humans compared to other primates

verfasst von: Kristen N. Hirter, Elaine N. Miller, Cheryl D. Stimpson, Kimberley A. Phillips, William D. Hopkins, Patrick R. Hof, Chet C. Sherwood, C. Owen Lovejoy, Mary Ann Raghanti

Erschienen in: Brain Structure and Function | Ausgabe 6/2021

Einloggen, um Zugang zu erhalten

Abstract

Recent evidence suggests that increased dopaminergic signaling within the dorsal striatum played a central role in the evolution of the human brain. This increase has been linked to human prosociality and language in what has been described as a dopamine-dominated striatum personality style. Increased striatal dopamine is associated with an increase in ventral striatal activity and promotes externally driven behaviors, including cooperation and social conformity. In contrast, decreased striatal dopamine is associated with increased dorsal striatal activity and favors internally driven and goal-oriented behaviors. Previous comparative studies have focused on the dorsal striatum, measuring dopaminergic innervation in the dorsal and medial caudate nucleus and putamen. Here, we add to this knowledge by examining regions of the ventral striatum. We quantified the density of tyrosine hydroxylase–immunoreactive axons, as a measure of dopaminergic innervation, in the nucleus accumbens and ventral pallidum of humans, great apes, platyrrhine and cercopithecid monkeys. Our data show that humans have a significantly greater dopaminergic innervation in both structures, supporting the hypothesis that selection for a prosocial neurochemistry in the human basal ganglia may have contributed to the evolution of our uniquely social behavior profile.
Literatur
Zurück zum Zitat Aragona BJ, Liu Y, Yu YJ, Curtis JT, Detwiler JM, Insel TR, Wang Z (2006) Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds. Nature Neurosci 9:133–139 PubMed Aragona BJ, Liu Y, Yu YJ, Curtis JT, Detwiler JM, Insel TR, Wang Z (2006) Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds. Nature Neurosci 9:133–139 PubMed
Zurück zum Zitat Arias-Carrión O, Stamelou M, Murillo-Rodriguez E, Menéndez-González M, Pöppel E (2010) Dopaminergic reward system: a short integrative review. Int Arch Med 3:24 PubMedPubMedCentral Arias-Carrión O, Stamelou M, Murillo-Rodriguez E, Menéndez-González M, Pöppel E (2010) Dopaminergic reward system: a short integrative review. Int Arch Med 3:24 PubMedPubMedCentral
Zurück zum Zitat Báez-Mendoza R, Harris CJ, Schultz W (2013) Activity of striatal neurons reflects social action and own reward. Proc Nat Acad Sci USA 110:16634–16639 PubMed Báez-Mendoza R, Harris CJ, Schultz W (2013) Activity of striatal neurons reflects social action and own reward. Proc Nat Acad Sci USA 110:16634–16639 PubMed
Zurück zum Zitat Bales KL, Mason WA, Catana C, Cherry SR, Mendoza SP (2007) Neural correltaes of pair-bonding in a monogamous primate. Brain Res 1184:245–253 PubMedPubMedCentral Bales KL, Mason WA, Catana C, Cherry SR, Mendoza SP (2007) Neural correltaes of pair-bonding in a monogamous primate. Brain Res 1184:245–253 PubMedPubMedCentral
Zurück zum Zitat Bergey CM, Phillips-Conroy JE, Disotell TR, Jolly CJ (2016) Dopamine pathway is highly diverged in primate species that differ markedly in social behavior. Proc Natl Acad Sci USA 113:6178–6181 PubMed Bergey CM, Phillips-Conroy JE, Disotell TR, Jolly CJ (2016) Dopamine pathway is highly diverged in primate species that differ markedly in social behavior. Proc Natl Acad Sci USA 113:6178–6181 PubMed
Zurück zum Zitat Calvey T (2019) Human self-domestication and the extended evolutionary synthesis of addiction: how humans evolved a unique vulnerability. Neuroscience 419:100–107 PubMed Calvey T (2019) Human self-domestication and the extended evolutionary synthesis of addiction: how humans evolved a unique vulnerability. Neuroscience 419:100–107 PubMed
Zurück zum Zitat Cools AR, Hendriks G, Korten J (1975) The acetylcholine-dopamine balance in the basal ganglia of rhesus monkeys and its role in dynamic, dystonic, dyskinetic, and epileptoid motor activities. J Neural Transm 36:91–105 PubMed Cools AR, Hendriks G, Korten J (1975) The acetylcholine-dopamine balance in the basal ganglia of rhesus monkeys and its role in dynamic, dystonic, dyskinetic, and epileptoid motor activities. J Neural Transm 36:91–105 PubMed
Zurück zum Zitat Cools AR, Brachten R, Heeren D, Willemen A, Ellenbroek B (1990) Search after neurobiological profile of individual-specific features of Wistar rats. Brain Res Bull 24:49–69 PubMed Cools AR, Brachten R, Heeren D, Willemen A, Ellenbroek B (1990) Search after neurobiological profile of individual-specific features of Wistar rats. Brain Res Bull 24:49–69 PubMed
Zurück zum Zitat Curtis JT, Liu Y, Aragona BJ, Wang Z (2006) Dopamine and monogamy. Brain Res 1126:76–90 PubMed Curtis JT, Liu Y, Aragona BJ, Wang Z (2006) Dopamine and monogamy. Brain Res 1126:76–90 PubMed
Zurück zum Zitat Filkowski MM, Cochran RN, Haas BW (2016) Altruistic behavior: mapping responses in the brain. Neurosci Neuroecon 5:65–75 PubMedPubMedCentral Filkowski MM, Cochran RN, Haas BW (2016) Altruistic behavior: mapping responses in the brain. Neurosci Neuroecon 5:65–75 PubMedPubMedCentral
Zurück zum Zitat Haber SN (2003) The primate basal ganglia: parallel and integrative networks. J Chem Neuroanat 26:317–330 PubMed Haber SN (2003) The primate basal ganglia: parallel and integrative networks. J Chem Neuroanat 26:317–330 PubMed
Zurück zum Zitat Haber SN, Knutson B (2010) The reward circuit: linking primate anatomy to human imaging. Neuropsychopharmacology 35:4–26 Haber SN, Knutson B (2010) The reward circuit: linking primate anatomy to human imaging. Neuropsychopharmacology 35:4–26
Zurück zum Zitat Haber SN, McFarland NR (1999) The concept of the ventral striatum in nonhuman primates. Ann NY Acad Sci 877:33–48 PubMed Haber SN, McFarland NR (1999) The concept of the ventral striatum in nonhuman primates. Ann NY Acad Sci 877:33–48 PubMed
Zurück zum Zitat Haber SN, Kunishio K, Mizobuchi M, Lynd-Balta E (1995) The orbital and medial prefrontal circuit through the primate basal ganglia. J Neurosci 15:4851–4867 PubMedPubMedCentral Haber SN, Kunishio K, Mizobuchi M, Lynd-Balta E (1995) The orbital and medial prefrontal circuit through the primate basal ganglia. J Neurosci 15:4851–4867 PubMedPubMedCentral
Zurück zum Zitat Haber SN, Kim K-S, Mailly P, Cazavara R (2006) Reward-related cortical inputs define a larger striatal region in primates that interface with associative cortical connections, providing a substrate for incentive-based learning. J Neurosci 26:8368–8376 PubMedPubMedCentral Haber SN, Kim K-S, Mailly P, Cazavara R (2006) Reward-related cortical inputs define a larger striatal region in primates that interface with associative cortical connections, providing a substrate for incentive-based learning. J Neurosci 26:8368–8376 PubMedPubMedCentral
Zurück zum Zitat Haug H (1987) Brain sizes, surfaces, and neuronal sizes of the cortex cerebri: a stereological investigation of man and his variability and a comparison with some mammals (primates, whales, marsupials, insectivores, and one elephant). Am J Anat 180:126–142 PubMed Haug H (1987) Brain sizes, surfaces, and neuronal sizes of the cortex cerebri: a stereological investigation of man and his variability and a comparison with some mammals (primates, whales, marsupials, insectivores, and one elephant). Am J Anat 180:126–142 PubMed
Zurück zum Zitat Hawkins A, Olszewski J (1957) Glia/nerve cell index for cortex of the whale. Science 126:76–77 PubMed Hawkins A, Olszewski J (1957) Glia/nerve cell index for cortex of the whale. Science 126:76–77 PubMed
Zurück zum Zitat Herculano-Houzel S (2014) The glia/neuron ratio: How it varies uniformly across brain structures and species and what it means for brain physiology and evolution. Glia 62:1377–1391 PubMed Herculano-Houzel S (2014) The glia/neuron ratio: How it varies uniformly across brain structures and species and what it means for brain physiology and evolution. Glia 62:1377–1391 PubMed
Zurück zum Zitat Higley JD, King ST Jr, Hasert MF, Champoux M, Suomi SJ, Linnoila M (1996) Stability of interindividual differences in serotonin function and its relationship to severe aggression and competent social behavior in rhesus macaque females. Neuropsychopharmacol 14:67–76 Higley JD, King ST Jr, Hasert MF, Champoux M, Suomi SJ, Linnoila M (1996) Stability of interindividual differences in serotonin function and its relationship to severe aggression and competent social behavior in rhesus macaque females. Neuropsychopharmacol 14:67–76
Zurück zum Zitat Holloway RL (1967) Tools and teeth: some speculations regarding canine reduction. Am Anthropol 69:63–67 Holloway RL (1967) Tools and teeth: some speculations regarding canine reduction. Am Anthropol 69:63–67
Zurück zum Zitat Hostetler CM et al (2017) Effects of pair bonding on dopamine D1 receptors in monogamous male titi monkeys ( Callicebus cupreus). Am J Primatol 79:e22612 Hostetler CM et al (2017) Effects of pair bonding on dopamine D1 receptors in monogamous male titi monkeys ( Callicebus cupreus). Am J Primatol 79:e22612
Zurück zum Zitat Inoue-Murayama M et al (2002) Variation of variable number of tandem repeat sequences in the 3′-untranslated region of primate dopamine transporter genes that affects reporter gene expression. Neurosci Lett 334:206–210 PubMed Inoue-Murayama M et al (2002) Variation of variable number of tandem repeat sequences in the 3′-untranslated region of primate dopamine transporter genes that affects reporter gene expression. Neurosci Lett 334:206–210 PubMed
Zurück zum Zitat Jolly CJ, Phillips-COnroy JE, Kaplan JR, Mann JJ (2008) Cerebrospinal fluid monoaminergic metabolites in wild Papio anubis and P. hamadryas are concordant with taxon-specific behavioral ontogeny. Int J Primatol 29:1549–1566 Jolly CJ, Phillips-COnroy JE, Kaplan JR, Mann JJ (2008) Cerebrospinal fluid monoaminergic metabolites in wild Papio anubis and P. hamadryas are concordant with taxon-specific behavioral ontogeny. Int J Primatol 29:1549–1566
Zurück zum Zitat Jolly CJ, Phillips-Conroy JE, Kaplan JR, Mann JJ (2013) Monoamine neurotransmitter metabolites in the cerebrospinal fluid of a group of hybrid baboons ( Papio hamadryas and P. anubis). Int J Primatol 34:836–858 Jolly CJ, Phillips-Conroy JE, Kaplan JR, Mann JJ (2013) Monoamine neurotransmitter metabolites in the cerebrospinal fluid of a group of hybrid baboons ( Papio hamadryas and P. anubis). Int J Primatol 34:836–858
Zurück zum Zitat Kalivas PW, Volkow ND (2005) The neural basis of addition: a pathology of motivation and choice. Am J Psychiatry 162:1403–1413 PubMed Kalivas PW, Volkow ND (2005) The neural basis of addition: a pathology of motivation and choice. Am J Psychiatry 162:1403–1413 PubMed
Zurück zum Zitat Klimecki OM, Leiberg S, Ricard M, Singer T (2014) Differential pattern of functional brain plasticity after compassion and empathy training. Soc Cogn Affect Neurosci 9:873–879 PubMed Klimecki OM, Leiberg S, Ricard M, Singer T (2014) Differential pattern of functional brain plasticity after compassion and empathy training. Soc Cogn Affect Neurosci 9:873–879 PubMed
Zurück zum Zitat Klucharev V, Hytönen K, Rijpkema M, Smidts A, Fernández G (2009) Reinforcement learning signal predicts social conformity. Neuron 61:140–151 PubMed Klucharev V, Hytönen K, Rijpkema M, Smidts A, Fernández G (2009) Reinforcement learning signal predicts social conformity. Neuron 61:140–151 PubMed
Zurück zum Zitat Lovejoy CO (2009) Reexamining human origins in light of Ardipithecus ramidus. Science 326:74e71-74e78 Lovejoy CO (2009) Reexamining human origins in light of Ardipithecus ramidus. Science 326:74e71-74e78
Zurück zum Zitat Lovejoy CO (2014) Ardipithecus and early human evolution in light of twenty-first-century developmental biology. J Anthropol Res 70:337–363 Lovejoy CO (2014) Ardipithecus and early human evolution in light of twenty-first-century developmental biology. J Anthropol Res 70:337–363
Zurück zum Zitat Mavridis I (2015) The role of the nucleus accumbens in psychiaric disorders. Psychiatriki 25:282–294 PubMed Mavridis I (2015) The role of the nucleus accumbens in psychiaric disorders. Psychiatriki 25:282–294 PubMed
Zurück zum Zitat McCollum LA, McCullumsmith RE, Roberts RC (2016) Tyrosine hydroxylase localization in the nucleus accumbens in schizophrenia. Brain Sruct Funct 221:4451–4458 McCollum LA, McCullumsmith RE, Roberts RC (2016) Tyrosine hydroxylase localization in the nucleus accumbens in schizophrenia. Brain Sruct Funct 221:4451–4458
Zurück zum Zitat Miller GM, Madras BK (2002) Polymorphisms in the 3’-untranslated region of human and monkey dopamine transporter genes affect reporter gene expression. Mol Psychiatry 7:44–55 PubMed Miller GM, Madras BK (2002) Polymorphisms in the 3’-untranslated region of human and monkey dopamine transporter genes affect reporter gene expression. Mol Psychiatry 7:44–55 PubMed
Zurück zum Zitat Nowak RM (1999) Walker’s primates of the world. The Johns Hopkins University Press, Baltimore Nowak RM (1999) Walker’s primates of the world. The Johns Hopkins University Press, Baltimore
Zurück zum Zitat O’Connell LA, Hofmann HA (2011) The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J Comp Neurol 519:3599–3639 PubMed O’Connell LA, Hofmann HA (2011) The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J Comp Neurol 519:3599–3639 PubMed
Zurück zum Zitat Paxinos G et al (2000) The rhesus monkey brain in stereotaxic coordinates. Academic Press, San Diego, CA Paxinos G et al (2000) The rhesus monkey brain in stereotaxic coordinates. Academic Press, San Diego, CA
Zurück zum Zitat Paxinos G, Watson C, Petrides M, Rosa M, Tokuno H (2012) The marmoset brain in stereotaxic coordinates. Academic Press/Elsevier Paxinos G, Watson C, Petrides M, Rosa M, Tokuno H (2012) The marmoset brain in stereotaxic coordinates. Academic Press/Elsevier
Zurück zum Zitat Raghanti MA, Stimpson CD, Marcinkiewicz JL, Erwin JM, Hof PR, Sherwood CC (2008) Cortical dopaminergic innervation among humans, chimpanzees, and macaque monkeys: a comparative study. Neuroscience 155:203–220 PubMedPubMedCentral Raghanti MA, Stimpson CD, Marcinkiewicz JL, Erwin JM, Hof PR, Sherwood CC (2008) Cortical dopaminergic innervation among humans, chimpanzees, and macaque monkeys: a comparative study. Neuroscience 155:203–220 PubMedPubMedCentral
Zurück zum Zitat Raghanti MA et al (2009) Species-specific distributions of tyrosine hydroxylase-immunoreactive neurons within the prefrontal cortex of anthropoid primates. Neuroscience 158:1551–1559 PubMed Raghanti MA et al (2009) Species-specific distributions of tyrosine hydroxylase-immunoreactive neurons within the prefrontal cortex of anthropoid primates. Neuroscience 158:1551–1559 PubMed
Zurück zum Zitat Raghanti MA et al (2016) Human-specific increase in dopaminergic innervation in a striatal region associated with speech and language: a comparative analysis of the primate basal ganglia. J Comp Neurol 524:2117–2129 PubMed Raghanti MA et al (2016) Human-specific increase in dopaminergic innervation in a striatal region associated with speech and language: a comparative analysis of the primate basal ganglia. J Comp Neurol 524:2117–2129 PubMed
Zurück zum Zitat Raleigh MJ, McGuire MT, Brammer GL, Pollack DB, Yuwiler A (1991) Serotonergic mechanisms promote dominance acquisition in adult male vervet monkeys. Brain Res 559:181–190 PubMed Raleigh MJ, McGuire MT, Brammer GL, Pollack DB, Yuwiler A (1991) Serotonergic mechanisms promote dominance acquisition in adult male vervet monkeys. Brain Res 559:181–190 PubMed
Zurück zum Zitat Rilling JK, Sanfey AG (2011) The neuroscience of social decision making. Annu Rev Psychol 62:23–48 PubMed Rilling JK, Sanfey AG (2011) The neuroscience of social decision making. Annu Rev Psychol 62:23–48 PubMed
Zurück zum Zitat Sherwood CC et al (2006) Evolution of increased glia-neuron ratios in the human frontal cortex. Proc Natl Acad Sci USA 103:13606–13611 PubMed Sherwood CC et al (2006) Evolution of increased glia-neuron ratios in the human frontal cortex. Proc Natl Acad Sci USA 103:13606–13611 PubMed
Zurück zum Zitat Smaers JB, Rohlf FJ (2016) Testing species’ deviation from allometric predictions using the phylogenetic regression. Evolution 70:1145–1149 PubMed Smaers JB, Rohlf FJ (2016) Testing species’ deviation from allometric predictions using the phylogenetic regression. Evolution 70:1145–1149 PubMed
Zurück zum Zitat Sousa AMM et al (2017) Molecular and cellular reorganization of neural circuits in the human lineage. Science 358:1027–1032 PubMedPubMedCentral Sousa AMM et al (2017) Molecular and cellular reorganization of neural circuits in the human lineage. Science 358:1027–1032 PubMedPubMedCentral
Zurück zum Zitat Stallen M, Sanfey AG (2015) The neuroscience of social conformity: implications for fundamental and applied research. Front Neurosci 9:337 PubMedPubMedCentral Stallen M, Sanfey AG (2015) The neuroscience of social conformity: implications for fundamental and applied research. Front Neurosci 9:337 PubMedPubMedCentral
Zurück zum Zitat Tachibana Y, Hikosaka O (2012) The primate central pallidum encodes expected reward value and regulates motor action. Neuron 76:826–837 PubMedPubMedCentral Tachibana Y, Hikosaka O (2012) The primate central pallidum encodes expected reward value and regulates motor action. Neuron 76:826–837 PubMedPubMedCentral
Zurück zum Zitat Tanaka SC, Doya K, Okada G, Ueda K, Okamoto Y, Yamawaki S (2004) Prediction of immediate and future rewards differentially recruits cortico-basal ganglia loops. Nature Neurosci 7:887–893 PubMed Tanaka SC, Doya K, Okada G, Ueda K, Okamoto Y, Yamawaki S (2004) Prediction of immediate and future rewards differentially recruits cortico-basal ganglia loops. Nature Neurosci 7:887–893 PubMed
Zurück zum Zitat van den Bos R (2015) The dorsal and ventral striatum play different roles in the programming of social behaviour: a tribute to Lex Cools. Behav Pharmacol 26:6–17 PubMed van den Bos R (2015) The dorsal and ventral striatum play different roles in the programming of social behaviour: a tribute to Lex Cools. Behav Pharmacol 26:6–17 PubMed
Zurück zum Zitat van den Bercken J, Cools AR (1982) Evidence for the role of the caudate nucleus in the sequential organization of behavior. Behav Brain Res 4:319–337 PubMed van den Bercken J, Cools AR (1982) Evidence for the role of the caudate nucleus in the sequential organization of behavior. Behav Brain Res 4:319–337 PubMed
Zurück zum Zitat Volkow ND, Morales M (2015) The brain on drugs: from reward to addiction. Cell 162:712–725 PubMed Volkow ND, Morales M (2015) The brain on drugs: from reward to addiction. Cell 162:712–725 PubMed
Zurück zum Zitat Young LJ, Wang Z (2004) The neurobiology of pair bonding. Nat Neurosci 7:1048–1054 PubMed Young LJ, Wang Z (2004) The neurobiology of pair bonding. Nat Neurosci 7:1048–1054 PubMed
Zurück zum Zitat Young LJ, Wang Z, Insel TR (1998) Neuroendocrine bases of monogamy. Trends Neurosci 2:71–75 Young LJ, Wang Z, Insel TR (1998) Neuroendocrine bases of monogamy. Trends Neurosci 2:71–75
Zurück zum Zitat Zaki J, Schirmer J, Mitchell JP (2011) Social influence modulates the neural computation of value. Psychol Sci 22:894–900 PubMed Zaki J, Schirmer J, Mitchell JP (2011) Social influence modulates the neural computation of value. Psychol Sci 22:894–900 PubMed
Metadaten
Titel
The nucleus accumbens and ventral pallidum exhibit greater dopaminergic innervation in humans compared to other primates
verfasst von
Kristen N. Hirter
Elaine N. Miller
Cheryl D. Stimpson
Kimberley A. Phillips
William D. Hopkins
Patrick R. Hof
Chet C. Sherwood
C. Owen Lovejoy
Mary Ann Raghanti
Publikationsdatum
25.05.2021
Verlag
Springer Berlin Heidelberg
Erschienen in
Brain Structure and Function / Ausgabe 6/2021
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-021-02300-0

Weitere Artikel der Ausgabe 6/2021

Brain Structure and Function 6/2021 Zur Ausgabe

Neu im Fachgebiet Neurologie

Newsletter

Bestellen Sie unseren kostenlosen Newsletter Update Neurologie und bleiben Sie gut informiert – ganz bequem per eMail.