The receptor architecture of the pigeons' nidopallium caudolaterale: An avian analogue to the mammalian prefrontal cortex

Brain Structure and Function

Volumn 216, Issue 3, 2011, Pages 239-254

  Herold, Christina ^a   Palomero Gallagher, Nicola ^b   Hellmann, Burkhard ^c   Kröner, Sven ^d   Theiss, Carsten ^c   Güntürkün, Onur ^c   Zilles, Karl ^a,b  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

^c RUHR UNIVERSITY BOCHUM   (Germany)

^d UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

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

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ALPHA 1 ADRENERGIC RECEPTOR; ALPHA 2 ADRENERGIC RECEPTOR; AMPA RECEPTOR; DOPAMINE 1 RECEPTOR; GLUTAMATE RECEPTOR; KAINIC ACID RECEPTOR; MUSCARINIC M1 RECEPTOR; MUSCARINIC M2 RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NICOTINIC RECEPTOR; SEROTONIN 1A RECEPTOR;

AGED; ANIMAL STRUCTURES; ANIMAL TISSUE; ARTICLE; AUTORADIOGRAPHY; BINDING SITE; COMPARATIVE ANATOMY; CONTROLLED STUDY; CONVERGENT EVOLUTION; FEMALE; HUMAN; HUMAN TISSUE; MALE; NEUROANATOMY; NIDOPALLIUM CAUDOLATERALE; NONHUMAN; PIGEON; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; RECEPTOR DENSITY; TELENCEPHALON; TISSUE DISTRIBUTION;

ANIMALS; AUTORADIOGRAPHY; COLUMBIDAE; DENSITOMETRY; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; RATS; RECEPTOR, MUSCARINIC M1; RECEPTOR, MUSCARINIC M2; RECEPTOR, SEROTONIN, 5-HT1A; RECEPTORS, ADRENERGIC; RECEPTORS, AMPA; RECEPTORS, DOPAMINE D1; RECEPTORS, GABA-A; RECEPTORS, KAINIC ACID; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, NEUROTRANSMITTER; RECEPTORS, NICOTINIC; SPECIES SPECIFICITY; TELENCEPHALON;

AVES; COLUMBA; MAMMALIA; RATTUS;

EID: 84655176621     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-011-0301-5     Document Type: Article

References (100)

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 23:997-1005
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 22:42-56 (Pubitemid 38515812)
3. Amunts K, Schleicher A, Zilles K (2007) Cytoarchitecture of the cerebral cortex-more than localization. NeuroImage 37:1061-1065 (Pubitemid 47385257)
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 8:269-277 (Pubitemid 28226163)
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 485:165-182 (Pubitemid 40488080)
6. Atoji Y, Wild JM (2009) Afferent and efferent projections of the central caudal nidopallium in the pigeon (Columba livia). J Comp Neurol 517:350-370
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 298:431-442 (Pubitemid 20274100)
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 9:121-133
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 492:163-175 (Pubitemid 19184548)
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 446:58-67 (Pubitemid 34252850)
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 20:523-529 (Pubitemid 27459658)
12. Bingman VP, Ioalé P, Casini G, Bagnoli P (1985) Dorsomedial forebrain ablations and home loft association behavior in homing pigeons. Brain Behav Evol 26:1-9 (Pubitemid 15007383)
13. Bird CD, Emery NJ (2010) Rooks perceive support relations similar to six-month-old babies. Proc Biol Sci 277:147-151
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 9:1262-1272
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 25:219-229 (Pubitemid 40292053)
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 98:211-218 (Pubitemid 29084444)
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 83:69-91 (Pubitemid 47464694)
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)
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 95:489-502 (Pubitemid 37441640)
20. Castelino CB, Schmidt MF (2010) What birdsong can teach us about the central noradrenergic system. J Chem Neuroanat 39:96-111
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 433:241-245
22. Colombo M, Broadbent NJ, Taylor CS, Frost N (2001) The role of the avian hippocampus in orientation in space and time. Brain Res 919:292-301 (Pubitemid 33042575)
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 8:10-11 (Pubitemid 36188566)
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 428:577-608
25. Csillag A, Montagnese CM (2005) Thalamotelencephalic organization in birds. Brain Res Bull 66:303-310 (Pubitemid 41247670)
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 172:101-115
27. Diekamp B, Kalt T, Güntürkün O (2002a) Working memory neurons in pigeons. J Neurosci 22:RC210
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 22:9573-9580 (Pubitemid 35356199)
29. Dietl MM, Palacios JM (1988) Neurotransmitter receptors in the avian brain. I. Dopamine receptors. Brain Res 439:354-359 (Pubitemid 18065723)
30. Dietl MM, Cortes R, Palacios JM (1988) Neurotransmitter receptors in the avian brain. II. Muscarinic cholinergic receptors. Brain Res 439:360-365 (Pubitemid 18065724)
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 141:357-369
32. Divac I, Mogensen J, Bjorklund A (1985) The prefrontal 'cortex' in the pigeon. Biochemical evidence. Brain Res 332:365-368 (Pubitemid 15108008)
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 83:763-779 (Pubitemid 28068897)
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 16:268-279 (Pubitemid 43100071)
35. Emery NJ, Clayton NS (2004) The mentality of crows: Convergent evolution of intelligence in corvids and apes. Science 306:1903-1907 (Pubitemid 39627847)
36. Farries MA (2001) The oscine song system considered in the context of the avian brain: Lessons learned from comparative neurobiology. Brain Behav Evol 58:80-100 (Pubitemid 34114118)
37. Fortune ES, Margoliash D (1995) Parallel pathways and convergence onto HVc and adjacent neostriatum of adult zebra finches (Taeniopygia guttata). J Comp Neurol 360:413-441
38. Gagliardo A, Divac I (1993) Effects of ablation of the presumed equivalent of the mammalian prefrontal cortex on pigeon homing. Behav Neurosci 107:280-288 (Pubitemid 23187279)
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 78:155-162 (Pubitemid 26252884)
40. Gagliardo A, Ioalé 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 13:1617-1624 (Pubitemid 32423347)
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) 191:509-517
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 397:231-250 (Pubitemid 28303357)
43. Goldman-Rakic PS (1999) The "psychic" neuron of the cerebral cortex. Ann N Y Acad Sci 868:13-26
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 10:2125-2138
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 125-152
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 106:3633-3638
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 38:133-143 (Pubitemid 127499784)
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 66:311-316 (Pubitemid 41247671)
49. Güntürkün O (2005b) The avian 'prefrontal cortex' and cognition. Curr Opin Neurobiol 15:686-693 (Pubitemid 41682310)
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 37:185-189 (Pubitemid 29244046)
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 96:125-133 (Pubitemid 28494130)
52. Harvey PH, Krebs JR (1990) Comparing brains. Science 249:140-146
53. Hasselmo ME, Stern CE (2006) Mechanisms underlying working memory for novel information. Trends Cogn Sci 10:487-493 (Pubitemid 44602572)
54. Henley JM, Barnard EA (1990) Autoradiographic distribution of binding sites for the non-NMDA receptor antagonist CNQX in chick brain. Neurosci Lett 116:17-22 (Pubitemid 20237129)
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 194:223-229
56. Horn G (1981) Neural mechanisms of learning: An analysis of imprinting in the domestic chick. Proc R Soc Lond B Biol Sci 213:101-137 (Pubitemid 12199646)
57. Horn G, Bradley P, McCabe BJ (1985) Changes in the structure of synapses associated with learning. J Neurosci 5:3161-3168 (Pubitemid 16182597)
58. Hunt GR, Gray RD (2003) Diversification and cumulative evolution in New Caledonian crow tool manufacture. Proc Biol Sci 270:867-874 (Pubitemid 36459721)
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 6:151-159
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 18:1506-1520 (Pubitemid 351882029)
61. Kalenscher T, Diekamp B, Güntürkün O (2003) Neural architecture of choice behaviour in a concurrent interval schedule. Eur J Neurosci 18:2627-2637 (Pubitemid 37452679)
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 84:521-535 (Pubitemid 43339123)
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 26:2293-2302 (Pubitemid 47620488)
64. Karten HJ (1969) The ascending auditory pathway in the pigeon (Columba livia). II. Telencephalic projections of the nucleus ovoidalis thalami. Brain Res 11:134-53
65. Karten H, Hodos W (1967) A stereotaxic atlas of the brain of the pigeon (Columba livia). The Johns Hopkins University Press, Baltimore
66. Kenward B,Weir AA, Rutz C, Kacelnik A (2005) Behavioural ecology: Tool manufacture by naive juvenile crows. Nature 433:121
67. Kirsch JA, Güntürkün O, Rose J (2008) Insight without cortex: Lessons from the avian brain. Conscious Cogn 17:475-483
68. Kohler EC, Riters LV, Chaves L, Bingman VP (1996) The muscarinic acetylcholine antagonist scopolamine impairs short-distance homing pigeon navigation. Physiol Behav 60:1057-1061 (Pubitemid 26336722)
69. Korzeniewska E, Güntürkün O (1990) Sensory properties and afferents of the N. dorsolateralis posterior thalami of the pigeon. J Comp Neurol 292:457-479 (Pubitemid 20061578)
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 407:228-260 (Pubitemid 29162774)
71. Leutgeb S, Husband S, Riters LV, Shimizu T, Bingman VP (1996) Telencephalic afferents to the caudolateral neostriatum of the pigeon. Brain Res 730:173-181 (Pubitemid 26305337)
72. Levy R, Goldman-Rakic PS (1999) Association of storage and processing functions in the dorsolateral prefrontal cortex of the nonhuman primate. J Neurosci 19:5149-5158 (Pubitemid 29270150)
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 289:247-259 (Pubitemid 19270587)
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 119:797-805 (Pubitemid 40934371)
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 15:187-200 (Pubitemid 28466786)
76. McNab F, Klingberg T (2008) Prefrontal cortex and basal ganglia control access to working memory. Nat Neurosci 11:103-107
77. Medina L, Reiner A (2000) Do birds possess homologues of mammalian primary visual, somatosensory and motor cortices? Trends Neurosci 23:1-12 (Pubitemid 30100305)
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 75:63-70
79. Merker B (1983) Silver staining of cell bodies by means of physical development. J Neurosci Methods 9:235-241 (Pubitemid 14217619)
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 395:380-404 (Pubitemid 28287368)
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 111:611-623 (Pubitemid 34521899)
82. Mitsacos A, Dermon CR, Stassi K, Kouvelas ED (1990) Localization of L-glutamate binding sites in chick brain by quantitative autoradiography. Brain Res 513:348-352 (Pubitemid 20132278)
83. Mogensen J, Divac I (1982) The prefrontal 'cortex' in the pigeon. Behavioral evidence. Brain Behav Evol 21:60-66 (Pubitemid 13195901)
84. Mrzljak L, Pappy M, Leranth C, Goldman-Rakic PS (1995) Cholinergic synaptic circuitry in the macaque prefrontal cortex. J Comp Neurol 357:603-617
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 99:695-703 (Pubitemid 351253229)
86. Palomero-Gallagher N, Zilles K (2004) Isocortex. In: Paxinos G (ed) The rat nervous system, 3rd edn edn. Acadamic Press, San Diego, pp 729-757
87. Palomero-Gallagher N, Mohlberg H, Zilles K, Vogt B (2008) Cytology and receptor architecture of human anterior cingulate cortex. J Comp Neurol 508:906-926 (Pubitemid 351695456)
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 30:2336-2355
89. Pinaud R, Mello CV (2007) GABA immunoreactivity in auditory and song control brain areas of zebra finches. J Chem Neuroanat 34:1-21 (Pubitemid 47002218)
90. Pollok B, Prior H, Güntürkün O (2000) Development of object permancence in the food storing magpie (Pica pica). J Comp Psychol 114:148-157
91. Prior H, Schwarz A, Güntürkün O (2008) Mirror-induced behavior in the magpie (Pica pica): Evidence of self-recognition. PLoS Biol 6:e202
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 424:409-438 (Pubitemid 30670442)
93. Rehkämper G, Zilles K (1991) Parallel evolution in mammalian and avian brains: Comparative cytoarchitectonic and cytochemical analysis. Cell Tissue Res 263:3-28
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 473:377-414 (Pubitemid 38580457)
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 286:409-426 (Pubitemid 19223569)
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 98:1-15 (Pubitemid 28566191)
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 412:469-487 (Pubitemid 29398704)
98. Robbins TW, Arnsten AF (2009) The neuropsychopharmacology of fronto-executive function: Monoaminergic modulation. Annu Rev Neurosci 32:267-287
99. Rose SP (2000) God's organism? The chick as a model system for memory studies. Learn Mem 7:1-17 (Pubitemid 30104228)
100. Rose J, Colombo M (2005) Neural correlates of executive control in the avian brain. PLoS Biol 3:e190