Journal of Comparative Physiology A

, Volume 171, Issue 6, pp 799–806 | Cite as

Lateralization and unilateral transfer of spatial memory in marsh tits

  • Nicky Clayton


The results reported in this paper demonstrate lateralization and transfer of spatial memory processing in an adult, food-storig bird. The technique of monocular occlusion was used to investigate lateralization and memory transfer in food-storing marsh tits (Parus palustris) for two tasks, food-storing and one-trial associative learning, which rely on one-trial learning for the spatial location of hidden food items. In the food-storing task, marsh tits had to return to the sites where they had previously stored a seed; in the one-trial associative learning task, the birds had to return to sites where they had been allowed to eat some, but not all, of a piece of peanut. For both spatial memory tasks, it was demonstrated that although the visual systems fed by both eyes are involved in short-term storage, the right eye system is associated with long-term storage, and that memories are transferred from the left to the right eye system between 3 and 24 h after memory formation.

Key words

Lateralization Memory processing One trial spatial memory tasks Food-storing birds Marshtits 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Adret P, Rogers LJ (1989) Sex difference in the visual projections of young chicks: a quantitative study of the thalamofugal pathway. Brain Res 478:59–73Google Scholar
  2. Andrew RJ (1991) The nature of behavioural lateralization in the chick. In: Andrew RJ (ed) Neural and behavioural plasticity. Oxford University Press, OxfordGoogle Scholar
  3. Bianki V (1983) Hemispheric specialisation of the animal brain for information processing principles. Int J Neurosci 25:195–205Google Scholar
  4. Bingman VP, Bagnoli P, Iote P, Casini G (1984) Homing behaviour of pigeons after telencephalic ablations. Brain Behav Evol 24:94–108Google Scholar
  5. Bossema I (1979) Jays and oaks: an eco-ethological study of a symbiosis. Behaviour 70:1–117Google Scholar
  6. Brodbeck DR, Burack OR, Shettleworth SJ (1992) One-trial associative memory in black-capped chickadees. J Exp Psychol Anim Behav Proc 18:12–21Google Scholar
  7. Catania C (1965) Interocular transfer of discrimination in the pigeon. J Exp Anal Behav 8:147–155Google Scholar
  8. Cipolla-Neto J, Horn G, McCabe B (1982) Hemispheric asymmetry and imprinting: The effect of sequential lesions to the hyperstriatum ventrale. J Exp Brain Res 48:22–27Google Scholar
  9. Clayton NS (1993) The ontogeny of food-storing and retrieval in marsh tits. Behaviour (in press)Google Scholar
  10. Clayton NS, Krebs JR (1992) Lateralization in Paridae: comparison of a storing and a non-storing species on a one-trial associative memory task. J Comp Physiol 171Google Scholar
  11. Cowan MW, Adamson L, Powell TPS (1961) An experimental study of the avian visual system. J Anat Lond 95:545–563Google Scholar
  12. Cynx J, Williams H, Nottebohm F (1992) Hemispheric differences in avian song discrimination. Proc Natl Acad Sci USA 89:1372–1375Google Scholar
  13. Fersen L von, Guntürkün O (1990) Visual memory lateralization in pigeons. Neuropsychologia 28:1–7Google Scholar
  14. Gaston K, Gaston MG (1984) Unilateral memory after binocular discrimination training: left hemisphere dominance in the chick? Brain Res 303:190–193Google Scholar
  15. Gilbert D, Patterson I, Rose SPR (1991) Dissociation of brain sites necessary for registration and storage of memory for a one-trial passive avoidance task in the chick. Behav Neurosci 105:553–561Google Scholar
  16. Graves JA, Goodale MA (1977) Failure of interocular transfer in the pigeon (Columba livia). Physiol Behav 19:425–428Google Scholar
  17. Green L, Brecha N, Gazzaniga MS (1978) Interocular transfer of simultaneous but not successive discriminations in the pigeon. Anim Learn Behav 6:261–264Google Scholar
  18. Guntürkün O (1991) The functional organization of the avian visual system. In: Andrew RJ (ed) Neural and behavioural plasticity. Oxford University Press, OxfordGoogle Scholar
  19. Hampton RR, Sherry DF (1992) How cache loss affects choise of cache site in black-capped chickadees. Behav Ecol (in press)Google Scholar
  20. Healy SD, Krebs JR (1993) Spatial memory in tits: Recalling a single positive location. Anim Learn Behav (in press)Google Scholar
  21. Hodos W (1969) Color discrimination deficits after lesions of the nucleus rotundus in pigeons. Brain Behav Evol 2:185–200Google Scholar
  22. Hodos W (1976) Vision and the visual system: a bird's eye view. Progr Psychobiol Physiol Psychol 6:29–62Google Scholar
  23. Hodos W, Karten HJ (1966) Brightness and pattern discrimination deficits in the pigeon after lesions of nucleus rotundus. Exp Brain Res 2:151–167Google Scholar
  24. Hodos W, Karten HJ (1974) Visual intensity and pattern discrimination deficits after lesions of the optic lobe in pigeons. Brain Behav Evol 9:165–194Google Scholar
  25. Horn G (1985) Memory, imprinting, and the brain. Clarendon Press, OxfordGoogle Scholar
  26. Horn G, McCabe BJ, Cipolla-Neto J (1982) Imprinting in the domestic chick: The role of each side of the hyperstriatum ventrale in acquisition and retention. J Exp Brain Res 53:91–98Google Scholar
  27. Karten HJ, Hodos W, Nauta WJH, Revzin AL (1973) Neural connections of the visual wulst of the avian telencephalon. Experimental studies in the pigeon (Columba livia) and owl (Speotyto cunicularia). J Comp Neurol 150:253–257Google Scholar
  28. Krebs JR (1990) Food-storing birds: Adaptive specialization in brain and behaviour? Phil Trans R Soc B 329:55–62Google Scholar
  29. Krebs JR, Sherry DF, Healy SD, Perry VH, Vaccarino AL (1989) Hippocampal specialization of food-storing birds. Proc Natl Acad Sci USA 86:1388–1392Google Scholar
  30. Krebs JR, Healy SD, Shettleworth S (1990a) Spatial memory of Paridae: Comparison of storing and non-storing species P. ater and P. major. Anim Behav 39:1127–1138Google Scholar
  31. Krebs JR, Hilton SC, Healy SD (1990b) Memory in food-storing birds: adaptive specialization in brain and behaviour? In: Edelman GM, Gall WE, Cowan WM (eds) Signal and sense: local and global order in perceptual maps. Neuroscience Institute, New YorkGoogle Scholar
  32. Krushinskya NL (1966) Some complex forms of feeding behaviour of nutcracker, Nucifraga caryocatactes, after removal of old cortex. Zhurnal Evoluzionni Biochimii y Fisiologgia II: 563–568Google Scholar
  33. Levine JJ (1945) Studies of the interrelations of central nervous structures in binocular vision. I. The lack of binocular transfer of visual discriminative habits acquired monocularly by the pigeon. Genet Psychol 67:105–129Google Scholar
  34. Nottebohm F (1971) Neural lateralization of vocal control in a songbird. I. Song. J Exp Zool 177:229–262Google Scholar
  35. Rashid M, Andrew RJ (1989) Right hemisphere advantage for topographical orientation in the domestic chick. Neuropsychologia 27:937–948Google Scholar
  36. Rawlins JNP (1985) Associations across time: The hippocampus as a temporary memory store. Behav Brain Sci 8:479–496Google Scholar
  37. Robinson RG (1979) Different behavioral and biochemical effects of right and left cerebral infarction in the rat. Science 205:707–710Google Scholar
  38. Rogers LJ (1989) Laterality in animals. J Comp Psychol 3:5–25Google Scholar
  39. Rogers LJ (1991) Development of lateralization. In: Andrew RJ (ed) Neural and behavioural plasticity. Oxford University Press, OxfordGoogle Scholar
  40. Rogers LJ, Sink HS (1987) Transient asymmetry in the projections of the rostral thalamus to the visual hyperstriatum, and reversal of its direction by light exposure. Exp Brain Res 70:378–398PubMedGoogle Scholar
  41. Sandi C, Rose SPR, Patterson TA (1992) Hippocampal lesions prevent recall of a passive avoidance task in day-old chicks. Neurosci Lett 141:255–258Google Scholar
  42. Sandi C, Patterson TA, Rose SPR (1993) Visual input and lateralization of brain function in learning in the chick. Neuroscience (in press)Google Scholar
  43. Sherry DF (1989) Food storing in the Paridae. Wilson Bull 10:289–304Google Scholar
  44. Sherry DF, Vaccarino AL (1989) Hippocampal aspiration disrupts cache recovery in black-capped chickadees. Behav Neurosci 103:308–318Google Scholar
  45. Sherry DF, Krebs JR, Cowie RJ (1981) Memory for the location of stored food in marsh tits. Anim Behav 29:1260–1266Google Scholar
  46. Sherry DF, Vaccarino AL, Buckenham K, Herz RS (1989) The hippocampal complex of food-storing birds. Brain Behav Evol 34:308–317Google Scholar
  47. Shettleworth SJ, Krebs JR (1982) How marsh tits find their hoards: roles of site preferences and spatial memory. J Exp Psychol Anim Behav Proc 8:354–375Google Scholar
  48. Shettleworth SJ, Krebs JR (1986) Stored and encountered seeds: A comparison of two spatial memory tasks in marsh tits and chickadees. J Exp Psychol Anim Behav Proc 12:248–257Google Scholar
  49. Stevens ATD, Krebs JR (1986) Retrieval of stored seeds by marsh tits Parus palustris in the field. Ibis. J Exp Psychol Anim Behav Proc 128:513–525Google Scholar
  50. Wallman J, Pettigrew JD (1985) Conjunctive and disjunctive saccades in two avian species with contrasting oculomotor strategies. J Neurosci 5:1418–1428Google Scholar
  51. Watanabe S (1986) Interocular transfer of learning in the pigeon: visuo-motor integration and separation of discriminanda and manipulanda. Behav Brain Res 19:227–232Google Scholar
  52. Watanabe S, Hodos W, Bessette BB, Shimizu T (1986) Interocular transfer in parallel visual pathways in pigeons. Brain Behav Evol 29:184–195Google Scholar

Copyright information

© Springer-Verlag 1993

Authors and Affiliations

  • Nicky Clayton
    • 1
  1. 1.Edward Grey Institute, Department of ZoologyOxford UniversityOxfordUK

Personalised recommendations