Advertisement

Experimental Brain Research

, Volume 159, Issue 4, pp 519–529 | Cite as

Responses of dorsal subicular neurons of rats during object exploration in an extended environment

  • Michael I. Anderson
  • Shane M. O’MaraEmail author
Research Article

Abstract

The subiculum receives a direct projection from the perirhinal cortex, a cortical area whose neurons are responsive to the novelty or familiarity of objects encountered in the environment. We made recordings of subicular neuronal activity while male adult Wistar rats conducted object exploration tasks, which have been previously shown to cause changes in the exploratory behaviour of rats and which are dependent upon the integrity of structures within the hippocampal formation. In the current study, the exploratory behaviour of the rats was also modified in a manner consistent with them perceiving the novelty and familiarity of the objects used as part of the apparatus. Subicular cell firing, however, appeared to correlate best not with object novelty or familiarity, but with the concurrent location and speed of the rats within the task environment. These findings are discussed in light of previously reported ‘object-responsive’ subicular firing correlates.

Keywords

Object exploration Object recognition Rat Single units Subiculum 

Notes

Acknowledgements

We thank Sean Commins (Dept. of Psychology, Trinity College, Ireland) and John Gigg (Optometry and Neuroscience, UMIST, UK) for helpful comments. The Wellcome Trust supported this work.

References

  1. Amaral DG, Witter MP (1989) The three-dimensional organisation of the hippocampal formation: a review of anatomical data. Neuroscience 31:571–591CrossRefPubMedGoogle Scholar
  2. Amaral DG, Witter MP (1995) Hippocampal formation. In: Paxinos G (ed) The rat nervous system, 2nd edn. Academic Press, New York, pp 443–493Google Scholar
  3. Amaral DG, Dolorfo C, Alvarez-Royo P (1991) Organisation of CA1 projections to the subiculum: a PHA-L analysis in the rat. Hippocampus 1:415–436PubMedGoogle Scholar
  4. Anderson MI, O’Mara SM (2003) Analysis of recordings of single-unit firing and population activity in the dorsal subiculum of unrestrained, freely moving rats. J Neurophys 90:655–665Google Scholar
  5. Barnes CA, McNaughton B, Mizumori SJ, Leonard BW, Lin LH (1990) Comparison of spatial and temporal characteristics of neuronal activity in sequential stages of hippocampal processing. Prog Brain Res 83:287–300PubMedGoogle Scholar
  6. Brown MW, Aggleton JP (2001) Recognition memory: what are the roles of the perirhinal cortex and hippocampus? Nat Rev Neurosci 2:51–61CrossRefPubMedGoogle Scholar
  7. Brown MW, Xiang JZ (1998) Recognition memory: neuronal substrates of the judgement of prior occurrence. Prog Neurobiol 55:149–189CrossRefPubMedGoogle Scholar
  8. Cressant A, Muller RU, Poucet B (1997) Failure of centrally placed objects to control the firing fields of hippocampal place cells. J Neurosci 17:2531–2542PubMedGoogle Scholar
  9. Eichenbaum H (1999) The hippocampus and mechanisms of declarative memory. Behav Brain Res 103:123–133CrossRefPubMedGoogle Scholar
  10. Galani R, Weiss I, Cassel JC, Kelche C (1998) Spatial memory, habituation, and reactions to spatial and nonspatial changes in rats with selective lesions of the hippocampus, the entorhinal cortex or the subiculum. Behav Brain Res 96:1–12CrossRefPubMedGoogle Scholar
  11. Gemmell C, O’Mara SM (1999) Medial prefrontal cortex lesions cause deficits in a variable-goal location task but not in object exploration. Behav Neurosci 113:465–474CrossRefPubMedGoogle Scholar
  12. Gobbo OL, O’Mara SM (2004a) Enriched-environment housing enhances performance on odor discrimination, object exploration and spatial learning tasks independently of transient global ischemia. Behav Brain Res 152:231–241CrossRefPubMedGoogle Scholar
  13. Gobbo OL, O’Mara SM (2004b) The selective cyclooxygenase-2 inhibitor celecoxib can enhance or aggravate functional recovery from kainic acid-induced neurodegeneration in a time of administration dependent manner: involvement of brain-derived neurotrophic factor. Neuroscience 125:317–327CrossRefPubMedGoogle Scholar
  14. Kosel KC, Van Hoesen GW, Rosene DL (1983) A direct projection from the perirhinal cortex (area 35) to the subiculum in the rat. Brain Res 269:347–351CrossRefPubMedGoogle Scholar
  15. Martin PD, Ono T (2000) Effects of reward anticipation, reward presentation, and spatial parameters on the firing of single neurons recorded in the subiculum and nucleus accumbens of freely moving rats. Behav Brain Res 116:23–38CrossRefPubMedGoogle Scholar
  16. McNaughton BL, Barnes CA, O’Keefe J (1983) The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp Brain Res 52:41–49PubMedGoogle Scholar
  17. Muir GM, Bilkey DK (2003) Theta- and movement velocity-related firing of hippocampal neurons is disrupted by lesions centered on the perirhinal cortex. Hippocampus 13:93–108CrossRefPubMedGoogle Scholar
  18. 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
  19. 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
  20. Muller RU, Kubie JL, Bostock EM, Taube JS, Quirk GJ (1991) Spatial firing correlates of neurons in the hippocampal formation of freely moving rats. In: Pollard J (ed) Brain and space. Oxford University Press, Oxford, pp 296–333Google Scholar
  21. Naber PA, Cabellero-Bleda M, Jorritsma-Byham B, Witter MP (1997) Parallel input to the hippocampal memory system through peri- and postrhinal cortices. Neuroreport 8:2617–2621PubMedGoogle Scholar
  22. Naber PA, Witter MP, da Silva FHL (1999) Perirhinal cortex input to the hippocampus in the rat: evidence for parallel pathways, both direct and indirect. A combined physiological and anatomical study. Eur J Neurosci 11:4119–4133CrossRefPubMedGoogle Scholar
  23. O’Keefe J (1979) A review of the hippocampal place cells. Prog Neurobiol 13:419–439CrossRefPubMedGoogle Scholar
  24. O’Keefe J (1999) Do hippocampal pyramidal cells signal non-spatial as well as spatial information? Hippocampus 9:352–364CrossRefPubMedGoogle Scholar
  25. O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Clarendon Press, OxfordGoogle Scholar
  26. O’Mara SM (1995) Spatially selective firing properties of hippocampal formation neurons in rodents and primates. Prog Neurobiol 45:253–274CrossRefPubMedGoogle Scholar
  27. O’Mara SM, Commins S, Anderson M, Gigg J (2001) The subiculum: a review of form, physiology and function. Prog Neurobiol 64:129–155CrossRefPubMedGoogle Scholar
  28. Paxinos G, Watson C (1996) The rat brain in stereotaxic coordinates, compact 3rd edn. Academic Press, San DiegoGoogle Scholar
  29. Poucet B (1989) Object exploration, habituation, and response to a spatial change in rats following septal or medial frontal cortical damage. Behav Neurosci 103:1009–1016CrossRefPubMedGoogle Scholar
  30. Redish AD, Touretzky DS (1997) Cognitive maps beyond the hippocampus. Hippocampus 7:15–35CrossRefPubMedGoogle Scholar
  31. Rolls ET, Miyashita Y, Cahusac PM, Kesner RP, Niki H, Feigenbaum JD, Bach L (1989) Hippocampal neurons in the monkey with activity related to the place in which a stimulus is shown. J Neurosci 9:1835–1845PubMedGoogle Scholar
  32. Samsonovich A, McNaughton BL (1997) Path integration and cognitive mapping in a continuous attractor neural network model. J Neurosci 17:5900–5920PubMedGoogle Scholar
  33. Save E, Poucet B, Foreman N, Buhot MC (1992) Object exploration and reactions to spatial and nonspatial changes in hooded rats following damage to parietal cortex or hippocampal formation. Behav Neurosci 106:447–456CrossRefPubMedGoogle Scholar
  34. Sharp PE (1997) Subicular cells generate similar spatial firing patterns in two geometrically and visually distinctive environments: comparison with hippocampal place cells. Behav Brain Res 85:71–92CrossRefPubMedGoogle Scholar
  35. Sharp PE (1999) Comparison of the timing of hippocampal and subicular spatial signals: implications for path integration. Hippocampus 9:158–172CrossRefPubMedGoogle Scholar
  36. 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
  37. Skaggs WE, McNaughton BL, Gothard KM, Markus EJ (1993) An information-theoretic approach to deciphering the hippocampal code. In: Hanson SJ, Cowan JD, Giles CL (eds) Advances in neural information processing 5. Morgan Kaufman, San Mateo, pp 1030–1037Google Scholar
  38. Wan H, Aggleton JP, Brown MW (1999) Different contributions of the hippocampus and perirhinal cortex to recognition memory. J Neurosci 19:1142–1148PubMedGoogle Scholar
  39. Winer BJ (1971) Statistical principles in experimental design, 2nd edn. McGraw-Hill, New YorkGoogle Scholar
  40. Witter MP, Groenewegen HJ, Lopes da Silva FH, Lohman AHM (1989) Functional organisation of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog Neurobiol 33:161–253CrossRefPubMedGoogle Scholar
  41. Xiang JZ, Brown MW (1998) Differential neuronal encoding of novelty, familiarity and recency in regions of the anterior temporal lobe. Neuropharmacology 37:657–676CrossRefPubMedGoogle Scholar
  42. Zhu XO, Brown MW (1995) Changes in neuronal activity related to the repetition and relative familiarity of visual stimuli in rhinal and adjacent cortex of the anaesthetised rat. Brain Res 689:101–110CrossRefPubMedGoogle Scholar
  43. Zhu XO, Brown MW, Aggleton JP (1995a) Neuronal signalling of information important to visual recognition memory in rat rhinal and neighbouring cortices. Eur J Neurosci 7:753–765PubMedGoogle Scholar
  44. Zhu XO, Brown MW, McCabe BJ, Aggleton JP (1995b) Effects of the novelty or familiarity of visual stimuli on the expression of the immediate early gene c-fos in rat brain. Neuroscience 69:821–829CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Department of Psychology and Trinity College Institute of NeuroscienceUniversity of Dublin, Trinity CollegeDublin Ireland

Personalised recommendations