Psychological Research

, Volume 76, Issue 2, pp 212–219 | Cite as

The convergent evolution of neural substrates for cognition



This review describes a case of convergence in the evolution of brain and cognition. Both mammals and birds can organize their behavior flexibly over time and evolved similar cognitive skills. The avian forebrain displays no lamination that corresponds to the mammalian neocortex; hence, lamination does not seem to be a requirement for higher cognitive functions. In mammals, executive functions are associated with the prefrontal cortex. The corresponding structure in birds is the nidopallium caudolaterale. Anatomic, neurochemical, electrophysiologic and behavioral studies show these structures to be highly similar, but not homologous. Thus, despite the presence (mammals) or the absence (birds) of a laminated forebrain, ‘prefrontal’ areas in mammals and birds converged over evolutionary time into a highly similar neural architecture. The neuroarchitectonic degrees of freedom to create different neural architectures that generate identical prefrontal functions seem to be very limited.



This work was funded by a grant (SFB 874) from the German Research Foundation (Deutsche Forschungsgemeinschaft, DFG).


  1. Allen, C., & Bekoff, M. (1997). Species of Mind. Cambridge: MIT.Google Scholar
  2. Baddeley, A. D., & Hitch, G. (1974). Working Memory. In G. H. Bower (Ed.), The Psychology of Learning and Motivation (pp. 47–90). San Diego: Academic Press.Google Scholar
  3. Barton, R. A., & Harvey, P. H. (2000). Mosaic evolution of brain structure in mammals. Nature, 405, 1055–1058.PubMedCrossRefGoogle Scholar
  4. Bast, T., Diekamp, D., Thiel, C., Schwarting, R. K. W., & Güntürkün, O. (2002). Microdialysis in the ‘Prefrontal Cortex’ and the striatum of pigeons (Columba livia): Evidence for dopaminergic volume transmission in the avian associative forebrain. The Journal of Comparative Neurology, 446, 58–67.PubMedCrossRefGoogle Scholar
  5. Bird C. D., Emery N. J. (2009). Insightful problem solving and creative tool modification by captive nontool-using rooks. Proceedings of the National Academy of Sciences, USA, 106, 10370–10375.Google Scholar
  6. Blackledge, T.A., Gillespie, R. G. (2004). Convergent evolution of behavior in an adaptive radiation of Hawaiian web-building spiders. Proceedings of the National Academy of Sciences, USA, 101:16228–16332.Google Scholar
  7. Browning, R., Bruce Overmier, J., & Colombo, M. (2011). Delay activity in avian prefrontal cortex—sample code or reward code? European Journal of Neuroscience, 33, 726–735.PubMedCrossRefGoogle Scholar
  8. Bugnyar, T., & Heinrich, B. (2005). Ravens, Corvus corax, differentiate between knowledgeable and ignorant competitors. Proceedings of the Royal Society of London, Series B: Biological Sciences, 272, 1641–1646.Google Scholar
  9. Clayton, N. S., Bussey, T. J., & Dickinson, A. (2003). Can animals recall the past and plan for the future? Nature Reviews Neuroscience, 4, 685–691.PubMedCrossRefGoogle Scholar
  10. Cnotka, J., Güntürkün, O., Rehkämper, G., Gray, R. D., & Hunt, G. R. (2008). Extraordinary large brains in tool-using New Caledonian Crows (Corvus moneduloides). Neuroscience Letters, 433, 241–245.PubMedCrossRefGoogle Scholar
  11. Deaner, R. O., van Schaik, C. P., & Johnson, V. (2006). Do some taxa have better domain-general cognition than others? A meta-analysis of non-human primate studies. Evolutionary Psychology, 4, 149–196.Google Scholar
  12. Diekamp, B., Gagliardo, A., & Güntürkün, O. (2002a). Nonspatial and subdivision-specific working memory deficits after selective lesions of the avian ‘prefrontal cortex’. The Journal of Neuroscience, 22, 9573–9580.PubMedGoogle Scholar
  13. Diekamp, B., Kalt, T., Güntürkün, O. (2002a). Working memory neurons in pigeons. The Journal of Neuroscience, 22 RC210, 1–5.Google Scholar
  14. Dunnett, S. B., Nathwani, F., & Brasted, P. J. (1999). Medial prefrontal and neostriatal lesions disrupt performance in an operant delayed alternation task in rats. Behavioural Brain Research, 106, 13–28.PubMedCrossRefGoogle Scholar
  15. Durstewitz, D., Kelc, M., & Güntürkün, O. (1999). A neurocomputational theory of the dopaminergic modulation of working memory functions. The Journal of Neuroscience, 19, 2807–2822.PubMedGoogle Scholar
  16. Durstewitz, D., Kröner, S., Hemmings, H. C., Jr, & Güntürkün, O. (1998). The dopaminergic innervation of the pigeon telencephalon: Distribution of DARPP-32 and cooccurrence with glutamate decarboxylase and tyrosine hydroxylase. Neuroscience, 83, 763–779.PubMedCrossRefGoogle Scholar
  17. Durstewitz, D., Seamans, J. K., & Sejnowski, T. J. (2000). Dopamine-mediated stabilization of delay-period activity in a network model of prefrontal cortex. Journal of Neurophysiology, 83, 1733–1750.PubMedGoogle Scholar
  18. Edinger, L., Wallenberg, A., Holmes, G. M. (1903). Untersuchungen über die vergleichende Anatomie des Gehirns. 3. Das Vorderhirn der Vögel. Abhandlungen der Senckenbergischen Gesellschaft, 20, 343–426.Google Scholar
  19. Emery, N. J., & Clayton, N. S. (2004). The mentality of crows: convergent evolution of intelligence in corvids and apes. Science, 306, 1903–1907.PubMedCrossRefGoogle Scholar
  20. Fersen von, L. & Güntürkün, O. (1990). Visual memory lateralization in pigeons. Neuropsychologia, 28, 1–7.Google Scholar
  21. Fersen von, L., Wynne, C. D., Delius, J. D., & Staddon, J. E. (1990). Deductive reasoning in pigeons. Naturwissenschaften, 77, 548–549.CrossRefGoogle Scholar
  22. Gehring, W. J. (2005). New perspectives on eye development and the evolution of eyes and photoreceptors. Journal of Heredity, 96, 171–184.PubMedCrossRefGoogle Scholar
  23. Güntürkün, O. (1997). Cognitive impairments after lesions of the neostriatum caudolaterale and its thalamic afferent: functional similarities to the mammalian prefrontal system? Journal of Brain Research, 38, 133–143.PubMedGoogle Scholar
  24. Güntürkün, O. (2005). The avian prefrontal cortex and cognition. Current Opinion in Neurobiology, 15, 686–693.PubMedCrossRefGoogle Scholar
  25. Güntürkün, O., & Durstewitz, D. (2001). Multimodal areas of the avian forebrain—blueprints for cognition? In G. Roth & M. Wullimann (Eds.), Brain Evolution and Cognition (pp. 431–450). Heidelberg: Spektrum Akademischer Verlag.Google Scholar
  26. Güntürkün, O., & Remy, M. (1990). The topographical projection of the nisthmi pars parvocellularis (Ipc) onto the tectum opticum in the pigeon. Neuroscience Letters, 111, 18–22.PubMedCrossRefGoogle Scholar
  27. Hartmann, B., & Güntürkün, O. (1998). Selective deficits in reversal learning after neostriatum caudolaterale lesions in pigeons—possible behavioral equivalencies to the mammalian prefrontal system. Behavioural Brain Research, 96, 125–133.PubMedCrossRefGoogle Scholar
  28. Harvey, P. H., & Krebs, J. R. (1990). Comparing brains. Science, 249, 140–146.PubMedCrossRefGoogle Scholar
  29. Honig, W. K. (1978). Studies of Working Memory in the Pigeon. In S. H. Hulse & W. K. Honig (Eds.), Cognitive Processes in Animal Behavior (pp. 211–248). New York: Hillsdale.Google Scholar
  30. Hunt, G. R., & Gray, R. D. (2003). Diversification and cumulative evolution in new Caledonian crow tool manufacture. Proceedings of the Royal Society of London, Series B: Biological Sciences, 270, 867–874.Google Scholar
  31. Iwaniuk, A. N., Dean, K. M., Nelson, J. E. (2004). A mosaic pattern characterizes the evolution of the avian brain. Proceedings of the Royal Society of London, Series B: Biological Sciences, 271, S148–S151.Google Scholar
  32. Jarvis, E. D., Güntürkün, O., Bruce, L. L., Csillag, A., Karten, H., Kuenzel, W., et al. (2005). Avian brains and a new understanding of vertebrate brain evolution. Nature Review Neuroscience, 6, 151–159.CrossRefGoogle Scholar
  33. Jerison, H. J. (1979). The evolution of diversity in brain size. In M. E. Hahn (Ed.), Development and Evolution of Brain Size (pp. 29–57). New York: Academic Press.Google Scholar
  34. 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. European Journal of Neuroscience, 26, 2293–2302.PubMedCrossRefGoogle Scholar
  35. Keverne, E. B., Martel, F. L., Nevison, C. M. (1996). Primate brain evolution: genetic and functional considerations, Proceedings of the Royal Society of London, Series B: Biological Sciences, 262, 689–696.Google Scholar
  36. Kirsch, J., Güntürkün, O., & Rose, J. (2008). Insight without cortex: Lessons from the avian brain. Consciousness and Cognition, 17, 475–483.PubMedCrossRefGoogle Scholar
  37. Kröner, S., Gottmann, K., Hatt H., Güntürkün, O. (2002). Cell types within the neostriatum caudolaterale of the chick: Intrinsic electrophysiological and anatomical properties. Neuroscience, 110, 495–473.Google Scholar
  38. 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. The Journal of Comparative Neurology, 407, 228–260.PubMedCrossRefGoogle Scholar
  39. Lefebvre, L., Reader, S. M., & Sol, D. (2004). Brains, innovations and evolution in birds and primates. Brain, Behavior and Evolution, 63, 233–246.PubMedCrossRefGoogle Scholar
  40. Lefebvre, L., & Sol, D. (2008). Brains, lifestyles and cognition: Are there general trends? Brain, Behavior and Evolution, 72, 135–144.PubMedCrossRefGoogle Scholar
  41. Machens, C. K., Romo, R., & Brody, C. D. (2005). Flexible control of mutual inhibition: a neural model of two-interval discrimination. Science, 307, 1121–1124.PubMedCrossRefGoogle Scholar
  42. Medina, L., & Reiner, A. (2000). Do birds possess homologues of mammalian primary visual, somatosensory and motor cortices? Trends in Neuroscience, 23, 1–12.CrossRefGoogle Scholar
  43. Mehlhorn, J., Rehkämper, G., Hunt, G. R., Gray, R., & Güntürkün, O. (2010). Tool making New Caledonian crows have larger associative brain areas. Brain, Behavior Evolution, 75, 63–70.CrossRefGoogle Scholar
  44. 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.PubMedCrossRefGoogle Scholar
  45. Pollok, B., Prior, H., & Güntürkün, O. (2000). Development of object-permanence in the food-storing magpie (Pica pica). Journal of Comparative Psychology, 114, 148–157.PubMedCrossRefGoogle Scholar
  46. Prior, H., Schwarz, A., & Güntürkün, O. (2008). Mirror-induced behaviour in the magpie (Pica pica): Evidence for self-recognition. PLoS Biology, 6, e202.PubMedCrossRefGoogle Scholar
  47. Puelles, L., Kuwana, E., Puelles, E., Bulfone, A., Shimamura, K., Keleher, J., Smiga, S., et al. (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. The Journal of Comparative Neurology, 424, 409–438.Google Scholar
  48. Reader, S. M., Laland, K. N. (2002). Social intelligence, innovation and enhanced brain size in primates. Proceedings of the National Academy of Sciences, USA, 99, 4436–4441.Google Scholar
  49. Rehkämper, G., Frahm, H. D., & Zilles, K. (1991). Quantitative development of brain and brain structures in birds (Galliformes und Passeriformis) compared to that in mammals (insectivores and primates). Brain Behavior Evolution, 37, 125–143.CrossRefGoogle Scholar
  50. Reiner, A., Perkel, D. J., Bruce, L. L., Butler, A. B., Csillag, A., Kuenzel, W., et al. (2004). Revised nomenclature for avian telencephalon and some related brainstem nuclei. The Journal of Comparative Neurology, 473, 377–414.PubMedCrossRefGoogle Scholar
  51. Rose, J., & Colombo, M. (2005). Neural correlates of executive control in the avian brain. PLoS Biology, 3, e190.PubMedCrossRefGoogle Scholar
  52. Rose, J., Güntürkün, O., Kirsch, J. (2009). Evolution of association pallial areas: in birds. In M. D. Binder, N. Hirokawa, & U. Windhorst (Eds.), Encyclopedia in Neuroscience (pp. 1215–1219). Springer: Berlin.Google Scholar
  53. Sawaguchi, T. (2001). The effects of dopamine and its antagonists on directional delay-period activity of prefrontal neurons in monkeys during an oculomotor delayed-response task. Neuroscience Research, 41, 115–128.PubMedCrossRefGoogle Scholar
  54. Sawaguchi, T., & Goldman-Rakic, P. S. (1991). D1 dopamine receptors in prefrontal cortex: Involvement in working memory. Science, 251, 947–950.PubMedCrossRefGoogle Scholar
  55. Schnabel, R., Metzger, M., Jiang, S., Hemmings, H. C., Jr, Greengard, P., & Braun, K. (1997). Localization of dopamine D1 receptors and dopaminoceptive neurons in the chick forebrain. The Journal of Comparative Neurology, 388, 146–168.PubMedCrossRefGoogle Scholar
  56. Schultz, W. (1998). Predictive reward signal of dopamine neurons. Journal of Neurophysiology, 80, 1–27.PubMedGoogle Scholar
  57. Seamans, J. K., Durstewitz, D., Christie, B.R., Stevens, C.F., Sejnowski, T.J. (2001). Dopamine D1/D5 receptor modulation of excitatory synaptic inputs to layer V prefrontal cortex neurons. Proceedings of the National Academy of Sciences, USA, 98, 301–306.Google Scholar
  58. Seamans, J. K., & Yang, C. R. (2004). The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Progress in Neurobiology, 74, 1–58.PubMedCrossRefGoogle Scholar
  59. Sol, D., Bacher, S., Reader, S. M., & Lefebvre, L. (2008). Brain size predicts the success of mammal species introduced into novel environments. American Naturalist, 172, S63–S71.PubMedCrossRefGoogle Scholar
  60. Sol, D., Duncan, R. P., Blackburn, T. M., Cassey, P., Lefebvre, L. (2005). Big brains, enhanced cognition, and response of birds to novel environments. Proceedings of the National Academy of Sciences, USA, 102, 5460–5465.Google Scholar
  61. Stephan, H., Baron, G., Frahm, H. D. (1988). Comparative size of brains and brain components. In: H. D. Steklis, J. Erwin (Eds.), Comparative Primate Biology (pp. 1–38). New York: Alan R. Liss.Google Scholar
  62. Taylor, A. H., Hunt, G. R., Holzhaider, J. C., & Gray, R. D. (2007). Spontaneous metatool us by New Caledonian crows. Current Biology, 17, 1504–1507.PubMedCrossRefGoogle Scholar
  63. Taylor, A. H., Hunt, G. R., Medina, F. S., Gray, R. D. (2009). Do New Caledonian crows solve physical problems through causal reasoning? Proceedings of the Royal Society of London, Series B: Biological Sciences, 276, 247–254.Google Scholar
  64. Vijayraghavan, S., Wang, M., Birnbaum, S. G., Williams, G. V., & Arnsten, A. F. (2007). Inverted-U dopamine D1 receptor actions on prefrontal neurons engaged in working memory. Nature Neuroscience, 10, 376–384.PubMedCrossRefGoogle Scholar
  65. Wake, D. B., Wake, M. H., & Specht, C. D. (2011). Homoplasy: From detecting pattern to determining process and mechanism of evolution. Science, 331, 1032–1035.PubMedCrossRefGoogle Scholar
  66. Watanabe, M., Kodama, T., & Hikosaka, K. (1997). Increase of extracellular dopamine in primate prefrontal cortex during a working memory task. Journal of Neurophysiology, 78, 2795–2798.PubMedGoogle Scholar
  67. Weir, A. A. S., Chappell, J., & Kacelnik, A. (2002). Shaping of hooks in New Caledonian crows. Science, 297, 981.PubMedCrossRefGoogle Scholar
  68. Wynne, B., & Güntürkün, O. (1995). The dopaminergic innervation of the forebrain of the pigeon (Columba livia): A study with antibodies against tyrosine hydroxylase and dopamine. The Journal of Comparative Neurology, 358, 1–19.CrossRefGoogle Scholar
  69. Yamazaki, Y., Aust, U., Huber, L., & Güntürkün, O. (2007). Lateralized cognition: Asymmetrical and complementary strategies of pigeons during discrimination of the “human” concept. Cognition, 104, 315–344.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Department of BiopsychologyInstitute of Cognitive Neuroscience, Faculty of PsychologyBochumGermany

Personalised recommendations