Advertisement

Journal of Comparative Physiology A

, Volume 190, Issue 12, pp 1047–1062 | Cite as

Spatial response properties of homing pigeon hippocampal neurons: correlations with goal locations, movement between goals, and environmental context in a radial-arm arena

  • Gerald E. HoughEmail author
  • Verner P. Bingman
Original Paper

Abstract

The amniote hippocampal formation plays an evolutionarily-conserved role in the neural representation of environmental space. However, species differences in spatial ecology nurture the expectation of species differences in how hippocampal neurons represent space. To determine the spatial response properties of homing pigeon (Columba livia) HFneurons, we recorded from isolated units in birds freely navigating a radial arena in search of food present at four goal locations. Fifty of 76 neurons displayed firing rate variations that could be placed into three response categories. Location cells (n=25) displayed higher firing rates at restricted locations in the arena space, often in proximity to goal locations. Path cells (n=13) displayed higher firing rates as a pigeon moved between a subset of goal locations. Arena-off cells (n=12) were more active when a pigeon was in a baseline holding space compared to inside the arena. Overall, reliability and coherence scores of the recorded neurons were lower compared to rat place cells. The differences in the spatial response profiles of pigeon hippocampal formation neurons, when compared to rats, provide a departure point for better understanding the relationship between spatial behavior and how hippocampal formation neurons participate in the representation of space.

Keywords

Avian telencephalon Columba livia Hippocampus Learning and memory Space 

Abbreviations

CA1

Ammon’s horn area 1

CA3

Ammon’s horn area 3

DL

Dorsolateral hippocampal formation

DM

Dorsomedial hippocampal formation

HF

Hippocampal formation

RI

Rate index

V

Ventral HF

VC

Ventrocentral HF

VL

Ventrolateral HF

VM

Ventromedial HF

Notes

Acknowledgements

The authors thank Meghan Kahn for assistance in all aspects of this study, Doug Nitz for data analysis assistance and contributions to the Matlab programming, and Jennifer J. Siegel for methodological discussions. This study was supported by NSF grant IBN0075891 to V.P.B. All procedures were performed under an approved protocol by BGSU’s Institutional Animal Care and Use Committee, and complied with the Principles of animal care publication no. 86-23, revised 1985 of the National Institutes of Health and also with current US law on the use of vertebrate animals.

References

  1. Alerstam T (1991) Ecological causes and consequences of bird orientation. EXS 60:202–225PubMedGoogle Scholar
  2. Berthold P (2001) Bird migration: a general survey, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  3. Biegler R (2003) Reading cognitive and other maps: how to avoid getting buried in thought. In: Jeffery KJ (ed) The neurobiology of spatial behavior. Oxford University Press, OxfordGoogle Scholar
  4. Bingman VP, Able KP (2002) Maps in birds: representational mechanisms and neural bases. Curr Opin Neurobiol 12:745–750CrossRefPubMedGoogle Scholar
  5. Bingman VP, Jones TJ (1994) Sun compass-based spatial learning impaired in homing pigeons with hippocampal lesions. J Neurosci 14:6687–6694PubMedGoogle Scholar
  6. Bingman VP, Hough GE II, Kahn MC, Siegel JJ (2003) The homing pigeon hippocampus and space: in search of adaptive specialization. Brain Behav Evol 62:117–127CrossRefPubMedGoogle Scholar
  7. Braithwaite VA, Guilford T (1991) Viewing familiar landscapes affects pigeon homing. Proc R Soc Lond B Biol Sci 245:183–186Google Scholar
  8. Burgess N, Recce M, O’Keefe J (1994) A model of hippocampal function. Neural Netw 7:1065–1081Google Scholar
  9. Chappell J (1997) An analysis of clock-shift experiments: is scatter increased and deflection reduced in clock-shifted homing pigeons? J Exp Biol 200:2269–2277PubMedGoogle Scholar
  10. Clayton NS (1998) Memory and the hippocampus in food-storing birds: a comparative approach. Neuropharmacology 37:441–452CrossRefGoogle Scholar
  11. Colombo M, Broadbent N (2000) Is the avian hippocampus a functional homologue of the mammalian hippocampus? Neurosci Biobehav Rev 24:465–484CrossRefPubMedGoogle Scholar
  12. Ekstrom AD, Kahana MJ, Vaplan JB, Fields TA, Isham EA, Newman EL, Fried I (2003) Cellular networks underlying human spatial navigation. Nature 425:184–188CrossRefPubMedGoogle Scholar
  13. Erichsen JT, Bingman VP, Krebs JR (1991) The distribution of neuropeptides in the dorsomedial telencephalon of the pigeon (Columba livia): a basis for regional subdivisions. J Comp Neurol 314:478–492PubMedGoogle Scholar
  14. Fenton AA, Muller RU (1998) Place cell discharge is extremely variable during individual passes of the rat through the firing field. Proc Natl Acad Sci U S A 95:3182–3187CrossRefPubMedGoogle Scholar
  15. Fenton AA, Wesierska M, Kaminsky Y, Bures J (1998) Both here and there: simultaneous expression of autonomous spatial memories in rats. Proc Natl Acad Sci U S A 95:11493–11498CrossRefPubMedGoogle Scholar
  16. Frank LM, Brown EN, Wilson MA (2001) A comparison of the firing properties of putative excitatory and inhibitory neurons from CA1 and the entorhinal cortex. J Neurophysiol 86:2029–2040PubMedGoogle Scholar
  17. Gagliardo A, Ioalé P, Bingman VP (1999) Homing in pigeons: the role of the hippocampal formation in the representation of landmarks used for navigation. J Neurosci 19:311–315PubMedGoogle Scholar
  18. Gagliardo A, Odetti F, Ioalé P (2001) Relevance of visual cues for orientation at familiar sites by homing pigeons: an experiment in a circular arena. Proc R Soc Lond B Biol Sci 268:2065–2070CrossRefPubMedGoogle Scholar
  19. Gothard KM, Skaggs WE, Moore KM, McNaughton BL (1996) Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task. J Neurosci 16:823–835Google Scholar
  20. Gray CM, Maldonado PE, Wilson M, McNaughton B (1995) Tetrodes markedly improve the reliability and yield of multiple single-unit isolation from multi-unit recordings in cat striate cortex. J Neurosci Methods 63:43–54CrossRefPubMedGoogle Scholar
  21. Hampton R, Sherry D, Shettleworth S, Khurgel M, Ivy G (1995) Hippocampal volume and food-storing behavior are related in parids. Brain Behav Evol 45:54–61PubMedGoogle Scholar
  22. Healy SD, Krebs JR (1993) Developmental of hippocampal specialisation in a food-storing bird. Behav Brain Res: 53:127–131Google Scholar
  23. Hollup SA, Molden S, Donnett JG, Moser MB, Moser EI (2001) Accumulation of hippocampal place fields at the goal location in an annular watermaze task. J Neurosci 21:1635–1644PubMedGoogle Scholar
  24. Hough GE, Bingman VP (2003) Neural responses of homing pigeon hippocampal neurons: goals, paths and locations. Program No. 557.1, Abstract Viewer/Itinerary Planner 2003. Society for Neuroscience, WashingtonGoogle Scholar
  25. Hough GE, Pang KCH, Bingman VP (2002) Intrahippocampal connections in the pigeon (Columba livia) as revealed by stimulation evoked field potentials. J Comp Neurol 452:297–309CrossRefPubMedGoogle Scholar
  26. Hunter WS (1911) Some labyrinth habits of the domestic pigeon. J Anim Behav 1:278–304Google Scholar
  27. Jeffery KJ, Anderson MI (2003) Dissociation of the geometric and contextual influences on place cells. Hippocampus 13:868–872CrossRefPubMedGoogle Scholar
  28. Jung MW, Wiener SI, McNaughton BL (1994) Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J Neurosci 14:7347–7356PubMedGoogle Scholar
  29. Kahn MC, Bingman VP (2004) Lateralization of spatial learning in the avian hippocampal formation. Behav Neurobiol 118:333–344CrossRefGoogle Scholar
  30. Kahn MC, Hough GE, Ten Eyck GR, Bingman VP (2003) Internal connectivity of the homing pigeon (Columba livia) hippocampal formation: an anterograde and retrograde tracer study. J Comp Neurol 459:127–141CrossRefPubMedGoogle Scholar
  31. Karten HJ, Hodos W (1967) A stereotaxic atlas of the brain of the pigeon (Columba livia). Johns Hopkins Press, BaltimoreGoogle Scholar
  32. Knierim JJ, Kudrimoti HS, McNaughton BL (1998) Interactions between idiothetic cues and external landmarks in the control of place cells and head direction cells. J Neurophysiol 80:425–446Google Scholar
  33. Kramer G (1952) Experiments on bird orientation. Ibis 94:265–285Google Scholar
  34. Krebs JR, Erichsen JT, Bingman VP (1991) The distribution of neurotransmitters and neurotransmitter-related enzymes in the dorsomedial telencephalon of the pigeon (Columba livia). J Comp Neurol 314:467–477PubMedGoogle Scholar
  35. Krebs JR, Clayton NS, Healy SD, Cristol DA, Patel SN, Jolliffe AR (1996) The ecology of the avian brain: food-storing memory and the hippocampus. Ibis 138:34–46Google Scholar
  36. Kubie JL, Muller RU, Bostock E (1990) Spatial firing properties of hippocampal theta cells. J Neurosci 10:1110–1123PubMedGoogle Scholar
  37. Maguire EA, Burgess N, Donnett JG, Frackowiak RS, Frith CD, O’Keefe J (1998) Knowing where and getting there: a human navigation network. Science 280:921–924CrossRefPubMedGoogle Scholar
  38. Markus EJ, Barnes CA, McNaughton BL, Gladden VL, Skaggs WE (1994) Spatial information content and reliability of hippocampal CA1 neurons: effects of visual input. Hippocampus 4:410–421PubMedGoogle Scholar
  39. McNaughton BL, O’Keefe J, Barnes CA (1983) The stereotrode: a new technique for simultaneous isolation of several single units in the central nervous system from multiple unit records. J Neurosci Methods 8:391–397CrossRefPubMedGoogle Scholar
  40. McNaughton BL, Barnes CA, Gerrard JL, Gothard K, Jung MW, Knierim JJ, Kudrimoti H, Qin Y, Skaggs WE, Suster M, Weaver KL (1996) Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J Exp Biol 199:173–185PubMedGoogle Scholar
  41. Mizumori SJ, Leutgeb S (2001) Directing place representation in the hippocampus. Rev Neurosci 12:347–363PubMedGoogle Scholar
  42. Morris RG, Garrud P, Rawlins JN, O’Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297:681–683PubMedGoogle Scholar
  43. Muller RU, Kubie JL (1987) The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J Neurosci 7:1951–1968PubMedGoogle Scholar
  44. Muller RU, Kubie JL (1989) The firing of hippocampal place cells predicts the future position of freely moving rats. J Neurosci 9:4101–4110PubMedGoogle Scholar
  45. Muller RU, Kubie JL, Ranck JB Jr (1987) Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J Neurosci 7:1935–1950PubMedGoogle Scholar
  46. Nitz DA, McNaughton BL (1999) Hippocampal EEG and unit activity responses to modulation of serotonergic median raphe neurons in the freely behaving rat. Learn Mem 6:153–167PubMedGoogle Scholar
  47. O’Keefe J (1976) Place units in the hippocampus of the freely moving rat. Exp Neurol 51:78–109CrossRefPubMedGoogle Scholar
  48. O’Keefe J, Burgess N (1996) Geometric determinants of the place fields of hippocampal neurons. Nature 381:425–428CrossRefPubMedGoogle Scholar
  49. O’Keefe J, Dostrovsky J (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34:171–175CrossRefPubMedGoogle Scholar
  50. Pisana M (1986) Cytoarchitecture and connectional organization in the telencephalic medial wall of the domestic chick (Gallus domesticus). PhD dissertation, University of SussexGoogle Scholar
  51. Quirk GJ, Muller RU, Kubie JL (1990) The firing of hippocampal place cells in the dark depends on the rat’s recent experience. J Neurosci 10:2008–2017PubMedGoogle Scholar
  52. Quirk GJ, Muller RU, Kubie JL, Ranck JB Jr (1992) The positional firing properties of medial entorhinal neurons: description and comparison with hippocampal place cells. J Neurosci 12:1945–1963PubMedGoogle Scholar
  53. Rehkämper G, Haase E, Frahm HD (1988) Allometric comparison of brain weight and brain structure volumes in different breeds of the domestic pigeon, Columba livia f.d. (fantails, homing pigeons, strassers). Brain Behav Evol 31:141–149PubMedGoogle Scholar
  54. Reiner A, Perkel DJ, Bruce L, Butler A, Csillag A, Kuenzel W, Medina L, Paxinos G, Shimizu T, Striedter G, Wild M, Ball GF, Durand S, Güntürkun O, Lee D, Mello CV, Powers A, White SA, Hough GE, 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 473:377–414CrossRefPubMedGoogle Scholar
  55. Rodríguez F, López JC, Vargas JP, Gómez Y, Broglio C, Salas C (2002) Conservation of spatial memory function in the pallial forebrain of reptiles and ray-finned fishes. J Neurosci 22:2894–2903PubMedGoogle Scholar
  56. Rolls ET (1999) Spatial view cells and the representation of place in the primate hippocampus. Hippocampus 9:467–480CrossRefPubMedGoogle Scholar
  57. Save E, Cressant A, Thinus-Blanc C, Poucet B (1998) Spatial firing of hippocampal place cells in blind rats. J Neurosci 18:1818–1826PubMedGoogle Scholar
  58. Schmidt-Koenig K, Ganzhorn JU, Ranvaud R (1991) Orientation in birds. The sun compass. EXS 60:1–15Google Scholar
  59. Shapiro ML, Tanila H, Eichenbaum H (1997) Cues that hippocampal place cells encode: dynamic and hierarchical representation of local and distal stimuli. Hippocampus 7:624–642CrossRefPubMedGoogle Scholar
  60. Sharp PE (1996) Multiple spatial/behavioral correlates for cells in the rat postsubiculum: multiple regression analysis and comparison to other hippocampal areas. Cereb Cortex 6:238–259PubMedGoogle Scholar
  61. Sharp PE (1999a) Comparison of the timing of hippocampal and subicular spatial signals: implications for path integration. Hippocampus 9:158–172CrossRefPubMedGoogle Scholar
  62. Sharp PE (1999b) Complimentary roles for hippocampal versus subicular/entorhinal place cells in coding place, context, and events. Hippocampus 9:432–443CrossRefPubMedGoogle Scholar
  63. Sharp PE (2002) The neural basis of navigation: evidence from single cell recordings. Kluwer, BostonGoogle Scholar
  64. Sharp PE, Green C (1994) Spatial correlates of firing patterns of single cells in the subiculum of the freely moving rat. J Neurosci 14:2339–2356PubMedGoogle Scholar
  65. Sharp PE, Blair HT, Etkin D, Tzanetos DB (1995) Influences of vestibular and visual motion information on the spatial firing patterns of hippocampal place cells. J Neurosci 15:173–189PubMedGoogle Scholar
  66. Sharp PE, Blair HT, Cho J (2001) The anatomical and computational basis of the rat head-direction cell signal. Trends Neurosci 24:289–294CrossRefPubMedGoogle Scholar
  67. Sherry DF, Vaccarino AL (1989) Hippocampus and memory for food cashes in black-capped chickadees. Behav Neurosci 103:308–318CrossRefGoogle Scholar
  68. Siegel JJ, Nitz D, Bingman VP (2000) Electrophysiological profile of avian hippocampal units: a comparative basis for regional subdivisions. Soc Neurosci Abstr 26:713Google Scholar
  69. Siegel JJ, Nitz D, Bingman VP (2002) Electrophysiological profile of avian hippocampal unit activity: a basis for regional subdivisions. J Comp Neurol 445:256–268CrossRefPubMedGoogle Scholar
  70. Siegel JJ, Nitz D, Bingman VP (2004) Spatial-specificity of single-units in the hippocampal formation of freely moving homing pigeons. Hippocampus (in press)Google Scholar
  71. Stackman RW, Clark AS, Taube JS (2002) Hippocampal spatial responses require vestibular input. Hippocampus 12:29–303CrossRefPubMedGoogle Scholar
  72. Szèkely AD (1999) The avian hippocampal formation: subdivisions and connectivity. Behav Brain Res 98:219–225CrossRefPubMedGoogle Scholar
  73. Taube JS (1995) Place cells recorded in the parasubiculum of freely moving rats. Hippocampus 5:569–583PubMedGoogle Scholar
  74. Taube JS, Muller RU, Ranck JB Jr (1990) Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J Neurosci 10:420–435Google Scholar
  75. Thompson LT, Best PJ (1990) Long-term stability of the place-field activity of single units recorded from the dorsal hippocampus of freely behaving rats. Brain Res 509:299–308CrossRefPubMedGoogle Scholar
  76. Tömböl T, Davies DC, Nemeth A, Alpar A, Sebesteny T (2000) A Golgi and a combined Golgi/GABA immunogold study of local circuit neurons in the homing pigeon hippocampus. Anat Embryol 201:181–196CrossRefGoogle Scholar
  77. Volman SF, Grubb TC Jr, Schuett KC (1997) Relative hippocampal volume in relation to food-storing behavior in four species of woodpeckers. Brain Behav Evol 49:110–120PubMedGoogle Scholar
  78. Wallace DG, Hines DJ, Pellis SM, Whishaw IQ (2002) Vestibular information is required for dead reckoning in the rat. J Neurosci 22:10009–10017PubMedGoogle Scholar
  79. White AR, Strasser R, Bingman VP (2002) Hippocampus lesions impair landmark array spatial learning in homing pigeons: a laboratory study. Neurobiol Learn Mem 78:65–78CrossRefPubMedGoogle Scholar
  80. Wood ER, Dudchenko PA, Eichenbaum H (1999) The global record of memory in hippocampal neuronal activity. Nature 397:613–616CrossRefPubMedGoogle Scholar
  81. Wylie DR, Glover RG, Aitchison JD (1999) Optic flow input to the hippocampal formation from the accessory optic system. J Neurosci 19:5514–5527PubMedGoogle Scholar
  82. Zeigler HP, Bischof HJ (1993) Vision, brain, and behavior in birds. MIT Press, CambridgeGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Department of Psychology and J.P. Scott Center for Neuroscience, Mind and BehaviorBowling Green State UniversityBowling GreenUSA
  2. 2.Department of Biological SciencesRowan UniversityGlassboroUSA

Personalised recommendations