Brain Structure and Function

, Volume 216, Issue 3, pp 239–254 | Cite as

The receptor architecture of the pigeons’ nidopallium caudolaterale: an avian analogue to the mammalian prefrontal cortex

  • Christina Herold
  • Nicola Palomero-Gallagher
  • Burkhard Hellmann
  • Sven Kröner
  • Carsten Theiss
  • Onur Güntürkün
  • Karl Zilles
Original Article

Abstract

The avian nidopallium caudolaterale is a multimodal area in the caudal telencephalon that is apparently not homologous to the mammalian prefrontal cortex but serves comparable functions. Here we analyzed binding-site densities of glutamatergic AMPA, NMDA and kainate receptors, GABAergic GABAA, muscarinic M1, M2 and nicotinic (nACh) receptors, noradrenergic α1 and α2, serotonergic 5-HT1A and dopaminergic D1-like receptors using quantitative in vitro receptor autoradiography. We compared the receptor architecture of the pigeons’ nidopallial structures, in particular the NCL, with cortical areas Fr2 and Cg1 in rats and prefrontal area BA10 in humans. Our results confirmed that the relative ratios of multiple receptor densities across different nidopallial structures (their “receptor fingerprints”) were very similar in shape; however, the absolute binding densities (the “size” of the fingerprints) differed significantly. This finding enables a delineation of the avian NCL from surrounding structures and a further parcellation into a medial and a lateral part as revealed by differences in densities of nACh, M2, kainate, and 5-HT1A receptors. Comparisons of the NCL with the rat and human frontal structures showed differences in the receptor distribution, particularly of the glutamate receptors, but also revealed highly conserved features like the identical densities of GABAA, M2, nACh and D1-like receptors. Assuming a convergent evolution of avian and mammalian prefrontal areas, our results support the hypothesis that specific neurochemical traits provide the molecular background for higher order processes such as executive functions. The differences in glutamate receptor distributions may reflect species-specific adaptations.

Keywords

Receptor autoradiography Prefrontal cortex Nidopallium caudolaterale Rat Human Fr2 Cg1 BA10 Dopamine Glutamate GABA 

Abbreviations

ACh

Acetylcholine

AMPA

α-Amino-3-hydroxy-5-methyl-4-isoxalone propionic acid

Cg1

Cingulate cortex 1

CDL

Dorsolateral corticoid area

EPSCs

Excitatory postsynaptic currents

FR2

Frontal area 2

GABA

γ-Aminobutyric acid

GLI

Gray level index

gluR1

Glutamate receptor subunit 1

HA

Hyperpallium apicale

HVC

Higher vocal center

IMM

Intermediate and medial mesopallium ventrale

MNH

Mediorostral nidopallium/hyperpallium

nACh

Nicotinic acetylcholine

NCC

Nidopallium caudocentrale

NCL

Nidopallium caudolaterale

NCLl

Nidopallium caudolaterale pars lateralis

NCLm

Nidopallium caudolaterale pars medialis

NCM

Nidopallium caudomediale

NFT

Nidopallium fronto-trigeminale

NIM

Nidopallium intermedium medialis

NMDA

N-methyl-d-aspartate

PFC

Prefrontal cortex

References

  1. Aamodt SM, Kozlowski MR, Nordeen EJ, Nordeen KW (1992) Distribution and developmental change in [3H]MK-801 binding within zebra finch song nuclei. J Neurobiol 23:997–1005PubMedCrossRefGoogle Scholar
  2. Amunts K, Weiss PH, Mohlberg H, Pieperhoff P, Eickhoff S, Gurd JM, Marshall JC, Shah JN, Fink GR, Zilles K (2004) Analysis of the neural mechanisms underlying verbal fluency in cytoarchitectonically defined stereotaxic space—the roles of Brodmann areas 44 and 45. NeuroImage 22:42–56PubMedCrossRefGoogle Scholar
  3. Amunts K, Schleicher A, Zilles K (2007) Cytoarchitecture of the cerebral cortex—more than localization. NeuroImage 37:1061–1065PubMedCrossRefGoogle Scholar
  4. Aoki C, Venkatesan C, Go CG, Forman R, Kurose H (1998) Cellular and subcellular sites for noradrenergic action in the monkey dorsolateral prefrontal cortex as revealed by the immunocytochemical localization of noradrenergic receptors and axons. Cereb Cortex 8:269–277PubMedCrossRefGoogle Scholar
  5. Atoji Y, Wild JM (2005) Afferent and efferent connections of the dorsolateral corticoid area and a comparison with connections of the temporo-parieto-occipital area in the pigeon (Columba livia). J Comp Neurol 485:165–182PubMedCrossRefGoogle Scholar
  6. Atoji Y, Wild JM (2009) Afferent and efferent projections of the central caudal nidopallium in the pigeon (Columba livia). J Comp Neurol 517:350–370PubMedCrossRefGoogle Scholar
  7. Ball GF, Nock B, Wingfield JC, McEwen BS, Balthazart J (1990) Muscarinic cholinergic receptors in the songbird and quail brain: a quantitative autoradiographic study. J Comp Neurol 298:431–442PubMedCrossRefGoogle Scholar
  8. Ball GF, Casto JM, Balthazart J (1995) Autoradiographic localization of D1-like dopamine receptors in the forebrain of male and female Japanese quail and their relationship with immunoreactive tyrosine hydroxylase. J Chem Neuroanat 9:121–133PubMedCrossRefGoogle Scholar
  9. Balthazart J, Ball GF (1989) Effects of the noradrenergic neurotoxin DSP-4 on luteinizing hormone levels, catecholamine concentrations, alpha 2-adrenergic receptor binding, and aromatase activity in the brain of the Japanese quail. Brain Res 492:163–175PubMedCrossRefGoogle Scholar
  10. Bast T, Diekamp B, Thiel C, Schwarting RK, Güntürkün O (2002) Functional aspects of dopamine metabolism in the putative prefrontal cortex analogue and striatum of pigeons (Columba livia). J Comp Neurol 446:58–67PubMedCrossRefGoogle Scholar
  11. Ben-Ari Y, Khazipov R, Leinekugel X, Caillard O, Gaiarsa JL (1997) GABAA, NMDA and AMPA receptors: a developmentally regulated ‘menage a trois’. Trends Neurosci 20:523–529PubMedCrossRefGoogle Scholar
  12. Bingman VP, Ioalè P, Casini G, Bagnoli P (1985) Dorsomedial forebrain ablations and home loft association behavior in homing pigeons. Brain Behav Evol 26:1–9PubMedCrossRefGoogle Scholar
  13. Bird CD, Emery NJ (2010) Rooks perceive support relations similar to six-month-old babies. Proc Biol Sci 277:147–151PubMedCrossRefGoogle Scholar
  14. Bock J, Schnabel R, Braun K (1997) Role of the dorso-caudal neostriatum in filial imprinting of the domestic chick: a pharmacological and autoradiographical approach focused on the involvement of NMDA-receptors. Eur J Neurosci 9:1262–1272PubMedCrossRefGoogle Scholar
  15. Bozkurt A, Zilles K, Schleicher A, Kamper L, Arigita ES, Uylings HB, Kötter R (2005) Distributions of transmitter receptors in the macaque cingulate cortex. Neuroimage 25:219–229PubMedCrossRefGoogle Scholar
  16. Braun K, Bock J, Metzger M, Jiang S, Schnabel R (1999) The dorsocaudal neostriatum of the domestic chick: a structure serving higher associative functions. Behav Brain Res 98:211–218PubMedCrossRefGoogle Scholar
  17. Briand LA, Gritton H, Howe WM, Young DA, Sarter M (2007) Modulators in concert for cognition: modulator interactions in the prefrontal cortex. Prog Neurobiol 83:69–91PubMedCrossRefGoogle Scholar
  18. Brodmann K (1909) Vergleichende Lokalisationslehre der Großhirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues, Barth, Leipzig; English translation available in Garey, L. J. Brodmann's Localization in the Cerebral Cortex (Smith Gordon, London, 1994)Google Scholar
  19. Callier S, Snapyan M, Le Crom S, Prou D, Vincent JD, Vernier P (2003) Evolution and cell biology of dopamine receptors in vertebrates. Biol Cell 95:489–502PubMedCrossRefGoogle Scholar
  20. Castelino CB, Schmidt MF (2010) What birdsong can teach us about the central noradrenergic system. J Chem Neuroanat 39:96–111PubMedCrossRefGoogle Scholar
  21. Cnotka J, Güntürkün O, Rehkämper G, Gray RD, Hunt GR (2008) Extraordinary large brains in tool-using New Caledonian crows (Corvus moneduloides). Neurosci Lett 433:241–245PubMedCrossRefGoogle Scholar
  22. Colombo M, Broadbent NJ, Taylor CS, Frost N (2001) The role of the avian hippocampus in orientation in space and time. Brain Res 919:292–301PubMedCrossRefGoogle Scholar
  23. Comings DE, Wu S, Rostamkhani M, McGue M, Lacono WG, Cheng LS, MacMurray JP (2003) Role of the cholinergic muscarinic 2 receptor (CHRM2) gene in cognition. Mol Psychiatry 8:10–11PubMedCrossRefGoogle Scholar
  24. Cornil C, Foidart A, Minet A, Balthazart J (2000) Immunocytochemical localization of ionotropic glutamate receptors subunits in the adult quail forebrain. J Comp Neurol 428:577–608PubMedCrossRefGoogle Scholar
  25. Csillag A, Montagnese CM (2005) Thalamotelencephalic organization in birds. Brain Res Bull 66:303–310Google Scholar
  26. de Almeida J, Palacios JM, Mengod G (2008) Distribution of 5-HT and DA receptors in primate prefrontal cortex: implications for pathophysiology and treatment. Prog Brain Res 172:101–115PubMedCrossRefGoogle Scholar
  27. Diekamp B, Kalt T, Güntürkün O (2002a) Working memory neurons in pigeons. J Neurosci 22:RC210PubMedGoogle Scholar
  28. Diekamp B, Gagliardo A, Güntürkün O (2002b) Nonspatial and subdivision-specific working memory deficits after selective lesions of the avian prefrontal cortex. J Neurosci 22:9573–9580PubMedGoogle Scholar
  29. Dietl MM, Palacios JM (1988) Neurotransmitter receptors in the avian brain. I. Dopamine receptors. Brain Res 439:354–359PubMedCrossRefGoogle Scholar
  30. Dietl MM, Cortes R, Palacios JM (1988) Neurotransmitter receptors in the avian brain. II. Muscarinic cholinergic receptors. Brain Res 439:360–365PubMedCrossRefGoogle Scholar
  31. Diez-Alarcia R, Pilar-Cuellar F, Paniagua MA, Meana JJ, Fernandez-Lopez A (2006) Pharmacological characterization and autoradiographic distribution of alpha2-adrenoceptor antagonist [3H]RX 821002 binding sites in the chicken brain. Neuroscience 141:357–369PubMedCrossRefGoogle Scholar
  32. Divac I, Mogensen J, Bjorklund A (1985) The prefrontal ‘cortex’ in the pigeon. Biochemical evidence. Brain Res 332:365–368PubMedCrossRefGoogle Scholar
  33. Durstewitz D, Kröner S, Hemmings HC Jr, Güntürkün O (1998) The dopaminergic innervation of the pigeon telencephalon: distribution of DARPP-32 and co-occurrence with glutamate decarboxylase and tyrosine hydroxylase. Neuroscience 83:763–779PubMedCrossRefGoogle Scholar
  34. Eickhoff S, Amunts K, Mohlberg H, Zilles K (2006) The human parietal operculum. II. Stereotaxic maps and correlation with functional imaging results. Cereb Cortex 16:268–279PubMedCrossRefGoogle Scholar
  35. Emery NJ, Clayton NS (2004) The mentality of crows: convergent evolution of intelligence in corvids and apes. Science 306:1903–1907PubMedCrossRefGoogle Scholar
  36. Farries MA (2001) The oscine song system considered in the context of the avian brain: lessons learned from comparative neurobiology. Brain Behav Evol 58:80–100PubMedCrossRefGoogle Scholar
  37. Fortune ES, Margoliash D (1995) Parallel pathways and convergence onto HVc and adjacent neostriatum of adult zebra finches (Taeniopygia guttata). J Comp Neurol 360:413–441PubMedCrossRefGoogle Scholar
  38. Gagliardo A, Divac I (1993) Effects of ablation of the presumed equivalent of the mammalian prefrontal cortex on pigeon homing. Behav Neurosci 107:280–288PubMedCrossRefGoogle Scholar
  39. Gagliardo A, Bonadonna F, Divac I (1996) Behavioural effects of ablations of the presumed ‘prefrontal cortex’ or the corticoid in pigeons. Behav Brain Res 78:155–162PubMedCrossRefGoogle Scholar
  40. Gagliardo A, Ioalè P, Odetti F, Bingman VP, Siegel JJ, Vallortigara G (2001) Hippocampus and homing in pigeons: left and right hemispheric differences in navigational map learning. Eur J Neurosci 13:1617–1624PubMedCrossRefGoogle Scholar
  41. Gebhard R, Zilles K, Schleicher A, Everitt BJ, Robbins TW, Divac I (1995) Parcellation of the frontal cortex of the New World monkey Callithrix jacchus by eight neurotransmitter-binding sites. Anat Embryol (Berl) 191:509–517CrossRefGoogle Scholar
  42. Geyer S, Matelli M, Luppino G, Schleicher A, Jansen Y, Palomero-Gallagher N, Zilles K (1998) Receptor autoradiographic mapping of the mesial motor and premotor cortex of the macaque monkey. J Comp Neurol 397:231–250PubMedCrossRefGoogle Scholar
  43. Goldman-Rakic PS (1999) The “psychic” neuron of the cerebral cortex. Ann N Y Acad Sci 868:13–26PubMedCrossRefGoogle Scholar
  44. Goldman-Rakic PS, Lidow MS, Gallager DW (1990) Overlap of dopaminergic, adrenergic, and serotoninergic receptors and complementarity of their subtypes in primate prefrontal cortex. J Neurosci 10:2125–2138PubMedGoogle Scholar
  45. Gonzalez-Burgos G, Kröner S, Seamans JK (2007) Cellular mechanisms of working memory and its modulation by dopamine in the prefrontal cortex of primates and rats. In: Tseng KY, Atzori M (eds) Monoaminergic Modulation of Cortical Excitability. Springer, Berlin, pp 125–152CrossRefGoogle Scholar
  46. Greenwood PM, Lin MK, Sundararajan R, Fryxell KJ, Parasuraman R (2009) Synergistic effects of genetic variation in nicotinic and muscarinic receptors on visual attention but not working memory. Proc Natl Acad Sci USA 106:3633–3638PubMedCrossRefGoogle Scholar
  47. Güntürkün O (1997) Cognitive impairments after lesions of the neostriatum caudolaterale and its thalamic afferent: functional similarities to the mammalian prefrontal system? J Brain Res 38:133–143Google Scholar
  48. Güntürkün O (2005a) Avian and mammalian “prefrontal cortices”: limited degrees of freedom in the evolution of the neural mechanisms of goal-state maintenance. Brain Res Bull 66:311–316PubMedCrossRefGoogle Scholar
  49. Güntürkün O (2005b) The avian ‘prefrontal cortex’ and cognition. Curr Opin Neurobiol 15:686–693PubMedCrossRefGoogle Scholar
  50. Güntürkün O, Kröner S (1999) A polysensory pathway to the forebrain of the pigeon: the ascending projections of the nucleus dorsolateralis posterior thalami (DLP). Eur J Morphol 37:185–189PubMedCrossRefGoogle Scholar
  51. Hartmann B, Güntürkün O (1998) Selective deficits in reversal learning after neostriatum caudolaterale lesions in pigeons: possible behavioral equivalencies to the mammalian prefrontal system. Behav Brain Res 96:125–133PubMedCrossRefGoogle Scholar
  52. Harvey PH, Krebs JR (1990) Comparing brains. Science 249:140–146PubMedCrossRefGoogle Scholar
  53. Hasselmo ME, Stern CE (2006) Mechanisms underlying working memory for novel information. Trends Cogn Sci 10:487–493PubMedCrossRefGoogle Scholar
  54. Henley JM, Barnard EA (1990) Autoradiographic distribution of binding sites for the non-NMDA receptor antagonist CNQX in chick brain. Neurosci Lett 116:17–22PubMedCrossRefGoogle Scholar
  55. Herold C, Diekamp B, Güntürkün O (2008) Stimulation of dopamine D1 receptors in the avian fronto-striatal system adjusts daily cognitive fluctuations. Behav Brain Res 194:223–229PubMedCrossRefGoogle Scholar
  56. Horn G (1981) Neural mechanisms of learning: an analysis of imprinting in the domestic chick. Proc R Soc Lond B Biol Sci 213:101–137PubMedCrossRefGoogle Scholar
  57. Horn G, Bradley P, McCabe BJ (1985) Changes in the structure of synapses associated with learning. J Neurosci 5:3161–3168PubMedGoogle Scholar
  58. Hunt GR, Gray RD (2003) Diversification and cumulative evolution in New Caledonian crow tool manufacture. Proc Biol Sci 270:867–874PubMedCrossRefGoogle Scholar
  59. Jarvis ED, Güntürkün O, Bruce L, Csillag A, Karten H, Kuenzel W, Medina L, Paxinos G, Perkel DJ, Shimizu T, Striedter G, Wild JM, Ball GF, Dugas-Ford J, Durand SE, Hough GE, Husband S, Kubikova L, Lee DW, Mello CV, Powers A, Siang C, Smulders TV, Wada K, White SA, Yamamoto K, Yu J, Reiner A, Butler AB (2005) Avian brains and a new understanding of vertebrate brain evolution. Nat Rev Neurosci 6:151–159PubMedCrossRefGoogle Scholar
  60. Ji XH, Cao XH, Zhang CL, Feng ZJ, Zhang XH, Ma L, Li BM (2008) Pre- and postsynaptic beta-adrenergic activation enhances excitatory synaptic transmission in layer V/VI pyramidal neurons of the medial prefrontal cortex of rats. Cereb Cortex 18:1506–1520PubMedCrossRefGoogle Scholar
  61. Kalenscher T, Diekamp B, Güntürkün O (2003) Neural architecture of choice behaviour in a concurrent interval schedule. Eur J Neurosci 18:2627–2637PubMedCrossRefGoogle Scholar
  62. Kalenscher T, Güntürkün O, Calabrese P, Gehlen W, Kalt T, Diekamp B (2005) Neural correlates of a default response in a delayed go/no-go task. J Exp Anal Behav 84:521–535PubMedCrossRefGoogle Scholar
  63. Karakuyu D, Herold C, Güntürkün O, Diekamp B (2007) Differential increase of extracellular dopamine and serotonin in the ‘prefrontal cortex’ and striatum of pigeons during working memory. Eur J Neurosci 26:2293–2302PubMedCrossRefGoogle Scholar
  64. Karten HJ (1969) The ascending auditory pathway in the pigeon (Columba livia). II. Telencephalic projections of the nucleus ovoidalis thalami. Brain Res 11:134–53Google Scholar
  65. Karten H, Hodos W (1967) A stereotaxic atlas of the brain of the pigeon (Columba livia). The Johns Hopkins University Press, BaltimoreGoogle Scholar
  66. Kenward B, Weir AA, Rutz C, Kacelnik A (2005) Behavioural ecology: tool manufacture by naive juvenile crows. Nature 433:121PubMedCrossRefGoogle Scholar
  67. Kirsch JA, Güntürkün O, Rose J (2008) Insight without cortex: lessons from the avian brain. Conscious Cogn 17:475–483PubMedCrossRefGoogle Scholar
  68. Kohler EC, Riters LV, Chaves L, Bingman VP (1996) The muscarinic acetylcholine antagonist scopolamine impairs short-distance homing pigeon navigation. Physiol Behav 60:1057–1061PubMedCrossRefGoogle Scholar
  69. Korzeniewska E, Güntürkün O (1990) Sensory properties and afferents of the N. dorsolateralis posterior thalami of the pigeon. J Comp Neurol 292:457–479PubMedCrossRefGoogle Scholar
  70. Kröner S, Güntürkün O (1999) Afferent and efferent connections of the caudolateral neostriatum in the pigeon (Columba livia): a retro- and anterograde pathway tracing study. J Comp Neurol 407:228–260PubMedCrossRefGoogle Scholar
  71. Leutgeb S, Husband S, Riters LV, Shimizu T, Bingman VP (1996) Telencephalic afferents to the caudolateral neostriatum of the pigeon. Brain Res 730:173–181PubMedGoogle Scholar
  72. Levy R, Goldman-Rakic PS (1999) Association of storage and processing functions in the dorsolateral prefrontal cortex of the nonhuman primate. J Neurosci 19:5149–5158PubMedGoogle Scholar
  73. Lidow MS, Gallager DW, Rakic P, Goldman-Rakic PS (1989) Regional differences in the distribution of muscarinic cholinergic receptors in the macaque cerebral cortex. J Comp Neurol 289:247–259PubMedCrossRefGoogle Scholar
  74. Lissek S, Güntürkün O (2005) Out of context: NMDA receptor antagonism in the avian ‘prefrontal cortex’ impairs context processing in a conditional discrimination task. Behav Neurosci 119:797–805PubMedCrossRefGoogle Scholar
  75. Martinez de la Torre M, Mitsacos A, Kouvelas ED, Zavitsanou K, Balthazart J (1998) Pharmacological characterization, anatomical distribution and sex differences of the non-NMDA excitatory amino acid receptors in the quail brain as identified by CNQX binding. J Chem Neuroanat 15:187–200PubMedCrossRefGoogle Scholar
  76. McNab F, Klingberg T (2008) Prefrontal cortex and basal ganglia control access to working memory. Nat Neurosci 11:103–107PubMedCrossRefGoogle Scholar
  77. Medina L, Reiner A (2000) Do birds possess homologues of mammalian primary visual, somatosensory and motor cortices? Trends Neurosci 23:1–12PubMedCrossRefGoogle Scholar
  78. Mehlhorn J, Hunt GR, Gray RD, Rehkämper G, Güntürkün O (2010) Tool-making new caledonian crows have large associative brain areas. Brain Behav Evol 75:63–70PubMedCrossRefGoogle Scholar
  79. Merker B (1983) Silver staining of cell bodies by means of physical development. J Neurosci Methods 9:235–241PubMedCrossRefGoogle Scholar
  80. Metzger M, Jiang S, Braun K (1998) Organization of the dorsocaudal neostriatal complex: a retrograde and anterograde tracing study in the domestic chick with special emphasis on pathways relevant to imprinting. J Comp Neurol 395:380–404PubMedCrossRefGoogle Scholar
  81. Metzger M, Jiang S, Braun K (2002) A quantitative immuno-electron microscopic study of dopamine terminals in forebrain regions of the domestic chick involved in filial imprinting. Neuroscience 111:611–623PubMedCrossRefGoogle Scholar
  82. Mitsacos A, Dermon CR, Stassi K, Kouvelas ED (1990) Localization of l-glutamate binding sites in chick brain by quantitative autoradiography. Brain Res 513:348–352PubMedCrossRefGoogle Scholar
  83. Mogensen J, Divac I (1982) The prefrontal ‘cortex’ in the pigeon. Behavioral evidence. Brain Behav Evol 21:60–66PubMedCrossRefGoogle Scholar
  84. Mrzljak L, Pappy M, Leranth C, Goldman-Rakic PS (1995) Cholinergic synaptic circuitry in the macaque prefrontal cortex. J Comp Neurol 357:603–617PubMedCrossRefGoogle Scholar
  85. Naito E, Scheperjans F, Eickhoff SB, Amunts K, Roland P, Zilles K, Ehrsson HH (2008) Cytoarchitectonic areas in human superior parietal lobule are functionally implicated by an illusion of bimanual interaction with an external object. J Neurophysiol 99:695–703PubMedCrossRefGoogle Scholar
  86. Palomero-Gallagher N, Zilles K (2004) Isocortex. In: Paxinos G (ed) The rat nervous system, 3rd edn edn. Acadamic Press, San Diego, pp 729–757Google Scholar
  87. Palomero-Gallagher N, Mohlberg H, Zilles K, Vogt B (2008) Cytology and receptor architecture of human anterior cingulate cortex. J Comp Neurol 508:906–926PubMedCrossRefGoogle Scholar
  88. Palomero-Gallagher N, Vogt B, Mayberg HS, Schleicher A, Zilles K (2009) Receptor architecture of human cingulate cortex: insights into the four-region neurobiological model. Hum Brain Mapp 30:2336–2355PubMedCrossRefGoogle Scholar
  89. Pinaud R, Mello CV (2007) GABA immunoreactivity in auditory and song control brain areas of zebra finches. J Chem Neuroanat 34:1–21PubMedCrossRefGoogle Scholar
  90. Pollok B, Prior H, Güntürkün O (2000) Development of object permancence in the food storing magpie (Pica pica). J Comp Psychol 114:148–157PubMedCrossRefGoogle Scholar
  91. Prior H, Schwarz A, Güntürkün O (2008) Mirror-induced behavior in the magpie (Pica pica): evidence of self-recognition. PLoS Biol 6:e202Google Scholar
  92. Puelles L, Kuwana E, Puelles E, Bulfone A, Shimamura K, Keleher J, Smiga S, Rubenstein JL (2000) Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr-1. J Comp Neurol 424:409–438PubMedCrossRefGoogle Scholar
  93. Rehkämper G, Zilles K (1991) Parallel evolution in mammalian and avian brains: comparative cytoarchitectonic and cytochemical analysis. Cell Tissue Res 263:3–28PubMedCrossRefGoogle Scholar
  94. Reiner A, Perkel DJ, Bruce LL, Butler AB, Csillag A, Kuenzel W, Medina L, Paxinos G, Shimizu T, Striedter G, Wild M, Ball GF, Durand S, Güntürkün O, Lee DW, Mello CV, Powers A, White SA, Hough G, Kubikova L, Smulders TV, Wada K, Dugas-Ford J, Husband S, Yamamoto K, Yu J, Siang C, Jarvis ED (2004) Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473:377–414PubMedCrossRefGoogle Scholar
  95. Richfield EK, Young AB, Penney JB (1989) Comparative distributions of dopamine D-1 and D-2 receptors in the cerebral cortex of rats, cats, and monkeys. J Comp Neurol 286:409–426PubMedCrossRefGoogle Scholar
  96. Riters LV, Bingman VP (1999) The effects of lesions to the caudolateral neostriatum on sun compass based spatial learning in homing pigeons. Behav Brain Res 98:1–15Google Scholar
  97. Riters LV, Erichsen JT, Krebs JR, Bingman VP (1999) Neurochemical evidence for at least two regional subdivisions within the homing pigeon (Columba livia) caudolateral neostriatum. J Comp Neurol 412:469–487PubMedCrossRefGoogle Scholar
  98. Robbins TW, Arnsten AF (2009) The neuropsychopharmacology of fronto-executive function: monoaminergic modulation. Annu Rev Neurosci 32:267–287PubMedCrossRefGoogle Scholar
  99. Rose SP (2000) God’s organism? The chick as a model system for memory studies. Learn Mem 7:1–17PubMedCrossRefGoogle Scholar
  100. Rose J, Colombo M (2005) Neural correlates of executive control in the avian brain. PLoS Biol 3:e190PubMedCrossRefGoogle Scholar
  101. Rose J, Schiffer AM, Dittrich L, Güntürkün O (2010) The role of dopamine in maintenance and distractability of attention in the “prefrontal cortex” of pigeons. Neuroscience 167:232–237PubMedCrossRefGoogle Scholar
  102. Sakaue M, Somboonthum P, Nishihara B, Koyama Y, Hashimoto H, Baba A, Matsuda T (2000) Postsynaptic 5-hydroxytryptamine (1A) receptor activation increases in vivo dopamine release in rat prefrontal cortex. Br J Pharmacol 129:1028–1034PubMedCrossRefGoogle Scholar
  103. Salvatierra NA, Torre RB, Arce A (1997) Learning and novelty induced increase of central benzodiazepine receptors from chick forebrain, in a food discrimination task. Brain Res 757:79–84PubMedCrossRefGoogle Scholar
  104. Santi A, Weise L (1995) The effects of scopolamine on memory for time in rats and pigeons. Pharmacol Biochem Behav 51:271–277PubMedCrossRefGoogle Scholar
  105. Sarter M, Bruno JP (2000) Cortical cholinergic inputs mediating arousal, attentional processing and dreaming: differential afferent regulation of the basal forebrain by telencephalic and brainstem afferents. Neuroscience 95:933–952PubMedCrossRefGoogle Scholar
  106. Sarter M, Parikh V, Howe WM (2009) nAChR agonist-induced cognition enhancement: integration of cognitive and neuronal mechanisms. Biochem Pharmacol 78:658–667PubMedCrossRefGoogle Scholar
  107. Schleicher A, Palomero-Gallagher N, Morosan P, Eickhoff SB, Kowalski T, de Vos K, Amunts K, Zilles K (2005) Quantitative architectural analysis: a new approach to cortical mapping. Anat Embryol (Berl) 210:373–386CrossRefGoogle Scholar
  108. Schnabel R, Metzger M, Jiang S, Hemmings HC Jr, Greengard P, Braun K (1997) Localization of dopamine D1 receptors and dopaminoceptive neurons in the chick forebrain. J Comp Neurol 388:146–168PubMedCrossRefGoogle Scholar
  109. Seed AM, Tebbich S, Emery NJ, Clayton NS (2006) Investigating physical cognition in rooks, Corvus frugilegus. Curr Biol 16:697–701PubMedCrossRefGoogle Scholar
  110. Sorenson EM, Chiappinelli VA (1992) Localization of 3H-nicotine, 125I-kappa-bungarotoxin, and 125I-alpha-bungarotoxin binding to nicotinic sites in the chicken forebrain and midbrain. J Comp Neurol 323:1–12PubMedCrossRefGoogle Scholar
  111. Stewart MG, Bourne RC, Chmielowska J, Kalman M, Csillag A, Stanford D (1988) Quantitative autoradiographic analysis of the distribution of [3H]muscimol binding to GABA receptors in chick brain. Brain Res 456:387–391PubMedCrossRefGoogle Scholar
  112. Stewart MG, Cristol D, Philips R, Steele RJ, Stamatakis A, Harrison E, Clayton N (1999) A quantitative autoradiographic comparison of binding to glutamate receptor sub-types in hippocampus and forebrain regions of a food-storing and a non-food-storing bird. Behav Brain Res 98:89–94PubMedCrossRefGoogle Scholar
  113. Taylor AH, Hunt GR, Medina FS, Gray RD (2009) Do New Caledonian crows solve physical problems through causal reasoning? Proc Biol Sci 276:247–254PubMedCrossRefGoogle Scholar
  114. Uylings HBM, Sanz-Arigita E, de Vos K, Smeets WJAJ, Pool CW, Amunts K, Rajkowska G, Zilles K (2000) The importance of a human 3D database and atlas for studies of prefrontal and thalamic functions. Progr Brain Res 126:357–368CrossRefGoogle Scholar
  115. Uylings HB, Groenewegen HJ, Kolb B (2003) Do rats have a prefrontal cortex? Behav Brain Res 146:3–17PubMedCrossRefGoogle Scholar
  116. Van De Werd HJ, Rajkowska G, Evers P, Uylings HB (2010) Cytoarchitectonic and chemoarchitectonic characterization of the prefrontal cortical areas in the mouse. Brain Struct Funct 214:339–353CrossRefGoogle Scholar
  117. Van Eden CG, Lamme VA, Uylings HB (1992) Heterotopic cortical afferents to the medial prefrontal cortex in the rat. A combined retrograde and anterograde tracer study. Eur J Neurosci 4:77–97PubMedCrossRefGoogle Scholar
  118. Veenman CL, Albin RL, Richfield EK, Reiner A (1994) Distributions of GABAA, GABAB, and benzodiazepine receptors in the forebrain and midbrain of pigeons. J Comp Neurol 344:161–189PubMedCrossRefGoogle Scholar
  119. Veenman CL, Wild JM, Reiner A (1995) Organization of the avian “corticostriatal” projection system: a retrograde and anterograde pathway tracing study in pigeons. J Comp Neurol 354:87–126PubMedCrossRefGoogle Scholar
  120. Vogt BA, Pandya DN (1987) Cingulate cortex of the rhesus monkey: II. Cortical afferents. J Comp Neurol 262:271–289PubMedCrossRefGoogle Scholar
  121. Waeber C, Dietl MM, Hoyer D, Palacios JM (1989) 5.HT1 receptors in the vertebrate brain. Regional distribution examined by autoradiography. Naunyn Schmiedebergs Arch Pharmacol 340:486–494PubMedGoogle Scholar
  122. Waldmann C, Güntürkün O (1993) The dopaminergic innervation of the pigeon caudolateral forebrain: immunocytochemical evidence for a ‘prefrontal cortex’ in birds? Brain Res 600:225–234PubMedCrossRefGoogle Scholar
  123. Wang M, Ramos BP, Paspalas CD, Shu Y, Simen A, Duque A, Vijayraghavan S, Brennan A, Dudley A, Nou E, Mazer JA, McCormick DA, Arnsten AF (2007) Alpha2A-adrenoceptors strengthen working memory networks by inhibiting cAMP-HCN channel signaling in prefrontal cortex. Cell 129:397–410PubMedCrossRefGoogle Scholar
  124. Williams GV, Castner SA (2006) Under the curve: critical issues for elucidating D1 receptor function in working memory. Neuroscience 139:263–276PubMedCrossRefGoogle Scholar
  125. Wynne B, Güntürkün O (1995) Dopaminergic innervation of the telencephalon of the pigeon (Columba livia): a study with antibodies against tyrosine hydroxylase and dopamine. J Comp Neurol 357:446–464PubMedCrossRefGoogle Scholar
  126. Yamamoto K, Reiner A (2005) Distribution of the limbic-system associated membran protein (LAMP) in pigeon forebrain and midbrain. J Comp Neurol 486:221–242PubMedCrossRefGoogle Scholar
  127. Yamasaki M, Matsui M, Watanabe M (2010) Preferential localization of muscarinic M1 receptor on dendritic shaft and spine of cortical pyramidal cells and its anatomical evidence for volume transmission. J Neurosci 30:4408–4418PubMedCrossRefGoogle Scholar
  128. Zahrt J, Taylor JR, Mathew RG, Arnsten AF (1997) Supranormal stimulation of D1 dopamine receptors in the rodent prefrontal cortex impairs spatial working memory performance. J Neurosci 17:8528–8535PubMedGoogle Scholar
  129. Zhang W, Yamada M, Gomeza J, Basile AS, Wess J (2002) Multiple muscarinic acetylcholine receptor subtypes modulate striatal dopamine release, as studied with M1–M5 muscarinic receptor knock-out mice. J Neurosci 22:6347–6352PubMedGoogle Scholar
  130. Zilles K (1985) The cortex of the rat, a stereotaxic atlas. Springer Verlag, BerlinGoogle Scholar
  131. Zilles K, Amunts K (2010) Centenary of Brodmann’s map—conception and fate. Nat Rev Neurosci 11:139–145PubMedCrossRefGoogle Scholar
  132. Zilles K, Schleicher A, Palomero-Gallagher N, Amunts K (2002a) Quantitative analysis of cyto- and receptor architecture of the human brain. In: Mazziotta JC, Toga A (eds) Brain mapping: the methods. Elsevier, Amsterdam, pp 573–602Google Scholar
  133. Zilles K, Palomero-Gallagher N, Grefkes C, Scheperjans F, Boy C, Amunts K, Schleicher A (2002b) Architectonics of the human cerebral cortex and transmitter receptor fingerprints: reconciling functional neuroanatomy and neurochemistry. Eur Neuropsychopharmacol 12:587–599PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Christina Herold
    • 1
  • Nicola Palomero-Gallagher
    • 2
  • Burkhard Hellmann
    • 3
  • Sven Kröner
    • 5
  • Carsten Theiss
    • 4
  • Onur Güntürkün
    • 3
  • Karl Zilles
    • 1
    • 2
  1. 1.C. and O. Vogt-Institute of Brain ResearchUniversity of DüsseldorfDüsseldorfGermany
  2. 2.Institute of Neuroscience and Medicine INM-2, Research Center JülichJülichGermany
  3. 3.Department of Biopsychology, Institute of Cognitive Neuroscience, Faculty of PsychologyRuhr-University BochumBochumGermany
  4. 4.Institute of Anatomy and Molecular Embryology, Faculty of MedicineRuhr-University BochumBochumGermany
  5. 5.School of Behavioral and Brain SciencesThe University of Texas at DallasRichardsonUSA

Personalised recommendations