Skip to main content
SpringerLink
Log in

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

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3a, b
Fig. 4a–c
Fig. 5
Fig. 6a, b
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Amaral DG, Witter MP (1989) The three-dimensional organisation of the hippocampal formation: a review of anatomical data. Neuroscience 31:571–591

    Article  CAS  PubMed  Google Scholar 

  • Amaral DG, Witter MP (1995) Hippocampal formation. In: Paxinos G (ed) The rat nervous system, 2nd edn. Academic Press, New York, pp 443–493

  • Amaral DG, Dolorfo C, Alvarez-Royo P (1991) Organisation of CA1 projections to the subiculum: a PHA-L analysis in the rat. Hippocampus 1:415–436

    CAS  PubMed  Google Scholar 

  • 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 90:655–665

    Google Scholar 

  • 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 83:287–300

    CAS  PubMed  Google Scholar 

  • Brown MW, Aggleton JP (2001) Recognition memory: what are the roles of the perirhinal cortex and hippocampus? Nat Rev Neurosci 2:51–61

    Article  CAS  PubMed  Google Scholar 

  • Brown MW, Xiang JZ (1998) Recognition memory: neuronal substrates of the judgement of prior occurrence. Prog Neurobiol 55:149–189

    Article  CAS  PubMed  Google Scholar 

  • Cressant A, Muller RU, Poucet B (1997) Failure of centrally placed objects to control the firing fields of hippocampal place cells. J Neurosci 17:2531–2542

    CAS  PubMed  Google Scholar 

  • Eichenbaum H (1999) The hippocampus and mechanisms of declarative memory. Behav Brain Res 103:123–133

    Article  CAS  PubMed  Google Scholar 

  • 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 96:1–12

    Article  CAS  PubMed  Google Scholar 

  • 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 113:465–474

    Article  CAS  PubMed  Google Scholar 

  • 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 152:231–241

    Article  CAS  PubMed  Google Scholar 

  • 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 125:317–327

    Article  CAS  PubMed  Google Scholar 

  • 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 269:347–351

    Article  CAS  PubMed  Google Scholar 

  • 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 116:23–38

    Article  CAS  PubMed  Google Scholar 

  • 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 52:41–49

    CAS  PubMed  Google Scholar 

  • Muir GM, Bilkey DK (2003) Theta- and movement velocity-related firing of hippocampal neurons is disrupted by lesions centered on the perirhinal cortex. Hippocampus 13:93–108

    Article  PubMed  Google Scholar 

  • Muller RU, Kubie JL (1987) The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J Neurosci 7:1951–1968

    CAS  PubMed  Google Scholar 

  • Muller RU, Kubie JL (1989) The firing of hippocampal place cells predicts the future position of freely moving rats. J Neurosci 9:4101–4110

    CAS  PubMed  Google Scholar 

  • 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 296–333

  • Naber PA, Cabellero-Bleda M, Jorritsma-Byham B, Witter MP (1997) Parallel input to the hippocampal memory system through peri- and postrhinal cortices. Neuroreport 8:2617–2621

    CAS  PubMed  Google Scholar 

  • 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 11:4119–4133

    Article  CAS  PubMed  Google Scholar 

  • O’Keefe J (1979) A review of the hippocampal place cells. Prog Neurobiol 13:419–439

    Article  PubMed  Google Scholar 

  • O’Keefe J (1999) Do hippocampal pyramidal cells signal non-spatial as well as spatial information? Hippocampus 9:352–364

    Article  PubMed  Google Scholar 

  • O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Clarendon Press, Oxford

  • O’Mara SM (1995) Spatially selective firing properties of hippocampal formation neurons in rodents and primates. Prog Neurobiol 45:253–274

    Article  PubMed  Google Scholar 

  • O’Mara SM, Commins S, Anderson M, Gigg J (2001) The subiculum: a review of form, physiology and function. Prog Neurobiol 64:129–155

    Article  PubMed  Google Scholar 

  • Paxinos G, Watson C (1996) The rat brain in stereotaxic coordinates, compact 3rd edn. Academic Press, San Diego

  • Poucet B (1989) Object exploration, habituation, and response to a spatial change in rats following septal or medial frontal cortical damage. Behav Neurosci 103:1009–1016

    Article  CAS  PubMed  Google Scholar 

  • Redish AD, Touretzky DS (1997) Cognitive maps beyond the hippocampus. Hippocampus 7:15–35

    Article  CAS  PubMed  Google Scholar 

  • 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 9:1835–1845

    CAS  PubMed  Google Scholar 

  • Samsonovich A, McNaughton BL (1997) Path integration and cognitive mapping in a continuous attractor neural network model. J Neurosci 17:5900–5920

    CAS  PubMed  Google Scholar 

  • 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 106:447–456

    Article  CAS  PubMed  Google Scholar 

  • 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 85:71–92

    Article  CAS  PubMed  Google Scholar 

  • Sharp PE (1999) Comparison of the timing of hippocampal and subicular spatial signals: implications for path integration. Hippocampus 9:158–172

    Article  CAS  PubMed  Google Scholar 

  • Sharp PE, Green C (1994) Spatial correlates of firing patterns of single cells in the subiculum of the freely moving rat. J Neurosci 14:2339–2356

    CAS  PubMed  Google Scholar 

  • 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 1030–1037

  • Wan H, Aggleton JP, Brown MW (1999) Different contributions of the hippocampus and perirhinal cortex to recognition memory. J Neurosci 19:1142–1148

    CAS  PubMed  Google Scholar 

  • Winer BJ (1971) Statistical principles in experimental design, 2nd edn. McGraw-Hill, New York

  • 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 33:161–253

    Article  CAS  PubMed  Google Scholar 

  • Xiang JZ, Brown MW (1998) Differential neuronal encoding of novelty, familiarity and recency in regions of the anterior temporal lobe. Neuropharmacology 37:657–676

    Article  CAS  PubMed  Google Scholar 

  • 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 689:101–110

    Article  CAS  PubMed  Google Scholar 

  • 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 7:753–765

    CAS  PubMed  Google Scholar 

  • 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 69:821–829

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Department of Psychology and Trinity College Institute of Neuroscience, University of Dublin, Trinity College, 2, Dublin , Ireland

    Michael I. Anderson & Shane M. O’Mara

Authors
  1. Michael I. Anderson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shane M. O’Mara
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shane M. O’Mara.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Anderson, M.I., O’Mara, S.M. Responses of dorsal subicular neurons of rats during object exploration in an extended environment. Exp Brain Res 159, 519–529 (2004). https://doi.org/10.1007/s00221-004-1977-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-004-1977-z

Keywords

Search

Navigation