Direct cortical input modulates plasticity and spiking in CA1 pyramidal neurons (original) (raw)

Nature volume 416, pages 736–740 (2002)Cite this article

Abstract

The hippocampus is necessary for the acquisition and retrieval of declarative memories1,2. The best-characterized sensory input to the hippocampus is the perforant path projection from layer II of entorhinal cortex (EC) to the dentate gyrus3,4. Signals are then processed sequentially in the hippocampal CA fields before returning to the cortex via CA1 pyramidal neuron spikes. There is another EC input—the temporoammonic (TA) pathway—consisting of axons from layer III EC neurons that make synaptic contacts on the distal dendrites of CA1 neurons3,5,6. Here we show that this pathway modulates both the plasticity and the output of the rat hippocampal formation. Bursts of TA activity can, depending on their timing, either increase or decrease the probability of Schaffer-collateral (SC)-evoked CA1 spikes. TA bursts can also significantly reduce the magnitude of synaptic potentiation at SC–CA1 synapses. The TA–CA1 synapse itself exhibits both long-term depression (LTD) and long-term potentiation (LTP). This capacity for bi-directional plasticity can, in turn, regulate the TA modulation of CA1 activity: LTP or LTD of the TA pathway either enhances or diminishes the gating of CA1 spikes and plasticity inhibition, respectively.

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References

  1. Morris, R. G. M., Garrud, P., Rawlins, J. N. P. & O'Keefe, J. Place navigation impaired in rats with hippocampal lesions. Nature 297, 681–683 (1982).
    Article ADS CAS Google Scholar
  2. Eichenbaum, H. A cortical–hippocampal system for declarative memory. Nature Rev. Neurosci. 1, 41–50 (2001).
    Article Google Scholar
  3. Witter, M. P., Groenewegen, H. J., Silva, F. H. L. D. & Lohman, A. H. Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog. Neurobiol. 33, 161–253 (1989).
    Article CAS Google Scholar
  4. Amaral, D. G. & Witter, M. P. The three-dimensional organisation of the hippocampus: a review of the anatomical data. Neuroscience 31, 571–591 (1989).
    Article CAS Google Scholar
  5. Cajal, S. R. The Structure of Ammon's Horn (ed. Thomas, C. C.) (Thomas, Springfield, Illinois, 1968).
    Google Scholar
  6. Steward, O. & Scoville, S. A. Cells of origin of entorhinal cortical affferents to the hippocampus and fascia dentate of the rat. J. Comp. Neurol. 169, 347–370 (1976).
    Article CAS Google Scholar
  7. Dvorak-Carbone, H. & Schuman, E. M. Long-term depression of temporoammonic-CA1 hippocampal synaptic transmission. J. Neurophysiol. 81, 1036–1044 (1999).
    Article CAS Google Scholar
  8. Dvorak-Carbone, H. & Schuman, E. M. Patterned activity in stratum lacunosum moleculare inhibits CA1 pyramidal neuron firing. J. Neurophysiol. 82, 3213–3222 (1999).
    Article CAS Google Scholar
  9. Empson, R. M. & Heineman, U. The perforant path projection to hippocampal area CA1 in the rat hippocampal–entorhinal cortex combined slice. J. Physiol. (Lond.) 484, 707–720 (1995).
    Article CAS Google Scholar
  10. Levy, W. B., Desmond, N. L. & Zhang, D. X. Perforant path activation modulates the induction of long-term potentiation of the Schaffer collateral–hippocampal CA1 response: theoretical and experimental analyses. Learn. Mem. 4, 510–518 (1998).
    Article CAS Google Scholar
  11. Chrobak, J. J. & Buzsaki, G. Gamma oscillations in the entorhinal cortex of the freely behaving rat. J. Neurosci. 18, 388–398 (1998).
    Article CAS Google Scholar
  12. Chrobak, J. J., Lorincz, A. & Buzsaki, G. Physiological patterns in the hippocampo-entorhinal cortex system. Hippocampus 10, 457–465 (2000).
    Article CAS Google Scholar
  13. Colbert, C. M. & Levy, W. B. Electrophysiological and pharmacological characterization of perforant path synapses in CA1: mediation by glutamate receptors. J. Neurophysiol. 68, 1–8 (1992).
    Article CAS Google Scholar
  14. Maccaferri, G. & McBain, C. J. Passive propagation of LTD to stratum oriens-alveus inhibitory neurons modulates the temporoammonic input to the hippocampal CA1 region. Neuron 15, 137–145 (1995).
    Article CAS Google Scholar
  15. Jarrard, L. E., Okaichi, H., Steward, O. & Goldschmidt, R. B. On the role of hippocampal connections in the performance of place and cue tasks: comparisons with damage to hippocampus. Behav. Neurosci. 98, 946–954 (1984).
    Article CAS Google Scholar
  16. Jarrard, L. E. What does the hippocampus really do? Behav. Brain. Res. 71, 1–10 (1995).
    Article CAS Google Scholar
  17. Muller, R. A quarter of a century of place cells. Neuron 17, 813–822 (1996).
    Article CAS Google Scholar
  18. McNaughton, B. L., Barnes, C. A., Meltzer, J. & Sutherland, R. J. Hippocampal granule cells are necessary for normal spatial learning but not for spatially-selective pyramidal cell discharge. Exp. Brain. Res. 76, 485–496 (1989).
    Article CAS Google Scholar
  19. Brun, V. H., Otnæss, M. K., Witter, M. P., Moser, M. B. & Moser, E. I. Place representation in hippocampal area CA1 in the absence of input from area CA3. Soc. Neurosci. Abstr. 31 (2001).

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Acknowledgements

We thank G. Laurent for critial reading of the manuscript. This work was supported by Fundacao para a Ciencia e Tecnologia (FCT)—Portugal and the Howard Hughes Medical Institute.

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  1. Caltech/Howard Hughes Medical Institute, Division of Biology, 216-76, Pasadena, 91125, California, USA
    Miguel Remondes & Erin M. Schuman

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  1. Miguel Remondes
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  2. Erin M. Schuman
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Correspondence toErin M. Schuman.

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Remondes, M., Schuman, E. Direct cortical input modulates plasticity and spiking in CA1 pyramidal neurons.Nature 416, 736–740 (2002). https://doi.org/10.1038/416736a

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