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Three-dimensional reconstruction of the axon arbor of a CA3 pyramidal cell recorded and filled in vivo

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Abstract

The three-dimensional intrahippocampal distribution of axon collaterals of an in vivo filled CA3c pyramidal cell was investigated. The neuron was filled with biocytin in an anesthetized rat and the collaterals were reconstructed with the aid of a NeuroLucida program from 48 coronal sections. The total length of the axon collaterals exceeded 0.5 m, with almost 40,000 synaptic boutons. The majority of the collaterals were present in the CA1 region (70.0%), whereas 27.6% constituted CA3 recurrent collaterals with the remaining minority of axons returning to the dentate gyrus. The axon arbor covered more than two thirds of the longitudinal axis of the hippocampus, and the terminals were randomly distributed both locally and distally from the soma. We suggest that the CA3 system can be conceptualized as a single-module, in which nearby and distant targets are contacted by the same probability (similar to a mathematically defined random graph). This arrangement, in combination with the parallel input granule cells and parallel output CA1 pyramidal cells, appears ideal for segregation and integration of information and memories.

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References

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

    Article  PubMed  CAS  Google Scholar 

  • Andersen P, Bliss TV, Lomo T, Olsen LI, Skrede KK (1969) Lamellar organization of hippocampal excitatory pathways. Acta Physiol Scand 76:4A–5A

    PubMed  CAS  Google Scholar 

  • Andersen P, Soleng AF, Raastad M (2000) The hippocampal lamella hypothesis revisited. Brain Res 886:165–171

    Article  PubMed  CAS  Google Scholar 

  • Buckmaster PS, Wenzel HJ, Kunkel DD, Schwartzkroin PA (1996) Axon arbors and synaptic connections of hippocampal mossy cells in the rat in vivo. J Comp Neurol 366:271–292

    Article  PubMed  CAS  Google Scholar 

  • Buhl DL, Buzsáki G (2005) Developmental emergence of hippocampal fast-field “ripple” oscillations in the behaving rat pups. Neuroscience 134:1423–1430

    Article  PubMed  CAS  Google Scholar 

  • Buzsáki G (1986) Hippocampal sharp waves: their origin and significance. Brain Res 398:242–252

    Article  PubMed  Google Scholar 

  • Buzsáki G, Leung LW, Vanderwolf CH (1983) Cellular bases of hippocampal EEG in the behaving rat. Brain Res 287:139–171

    PubMed  Google Scholar 

  • Buzsáki G, Horvath Z, Urioste R, Hetke J, Wise K (1992) High-frequency network oscillation in the hippocampus. Science 256:1025–1027

    Article  PubMed  Google Scholar 

  • Csicsvári J, Jamieson B, Wise KD, Buzsáki G (2003) Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37:311–322

    Article  PubMed  Google Scholar 

  • Finch DM, Nowlin NL, Babb TL (1983) Demonstration of axonal projections of neurons in the rat hippocampus and subiculum by intracellular injection of HRP. Brain Res 271:201–216

    Article  PubMed  CAS  Google Scholar 

  • Grossman Y, Parnas I, Spira ME (1979) Differential conduction block in branches of a bifurcating axon. J Physiol 295:283–305

    PubMed  CAS  Google Scholar 

  • Hampson RE, Simeral JD, Deadwyler SA (1999) Distribution of spatial and nonspatial information in dorsal hippocampus. Nature 402:610–614

    Article  PubMed  CAS  Google Scholar 

  • Hasselmo ME, Bodelon C, Wyble BP (2002) A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comput 14:793–817

    Article  PubMed  Google Scholar 

  • Ishizuka N, Weber J, Amaral DG (1990) Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J Comp Neurol 295:580–623

    Article  PubMed  CAS  Google Scholar 

  • Jefferys JG (1995) Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions. Physiol Rev 75:689–723

    PubMed  CAS  Google Scholar 

  • Kanerva P (1988) Sparse distributed memory. The MIT Press, Cambridge

    Google Scholar 

  • Konopacki J, Bland BH, Roth SH (1988) Carbachol-induced EEG ‘theta’ in hippocampal formation slices: evidence for a third generator of theta in CA3c area. Brain Res 451:33–42

    Article  PubMed  CAS  Google Scholar 

  • Li XG, Somogyi P, Ylinen A, Buzsáki G (1994) The hippocampal CA3 network: an in vivo intracellular labeling study. J Comp Neurol 339:181–208

    Article  PubMed  CAS  Google Scholar 

  • Lőrincz A, Buzsáki G (2000) Two-phase computational model training long-term memories in the entorhinal-hippocampal region. Ann N Y Acad Sci 911:83–111

    Article  PubMed  Google Scholar 

  • Luscher HR, Shiner JS (1990a) Computation of action potential propagation and presynaptic bouton activation in terminal arborizations of different geometries. Biophys J 58:1377–1388

    Article  PubMed  CAS  Google Scholar 

  • Luscher HR, Shiner JS (1990b) Simulation of action potential propagation in complex terminal arborizations. Biophys J 58:1389–1399

    PubMed  CAS  Google Scholar 

  • Martin SJ, Clark RE (2007) The rodent hippocampus and spatial memory: from synapses to systems. Cell Mol Life Sci 64:401–431

    Article  PubMed  CAS  Google Scholar 

  • McNaughton BL, Morris RGM (1987) Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 10:408–415

    Article  Google Scholar 

  • McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser MB (2006) Path integration and the neural basis of the ‘cognitive map’. Nat Rev Neurosci 7:663–678

    Article  PubMed  CAS  Google Scholar 

  • Miles R, Wong RK (1983) Single neurones can initiate synchronized population discharge in the hippocampus. Nature 306:371–373

    Article  PubMed  CAS  Google Scholar 

  • Muller RU, Stead M, Pach J (1996) The hippocampus as a cognitive graph. J Gen Physiol 107:663–694

    Article  PubMed  CAS  Google Scholar 

  • Paxinos G, Watson C (1982) The rat brain in stereotaxic coordinates. Academic, Sidney

    Google Scholar 

  • Redish AD, Rosenzweig ES, Bohanick JD, McNaughton BL, Barnes CA (2000) Dynamics of hippocampal ensemble activity realignment: time versus space. J Neurosci 20:9298–9309

    PubMed  CAS  Google Scholar 

  • Shepherd GM, Harris KM (1998) Three-dimensional structure and composition of CA3→CA1 axons in rat hippocampal slices: implications for presynaptic connectivity and compartmentalization. J Neurosci 18:8300–8310

    PubMed  CAS  Google Scholar 

  • Sík A, Tamamaki N, Freund TF (1993) Complete axon arborization of a single CA3 pyramidal cell in the rat hippocampus, and its relationship with postsynaptic parvalbumin-containing interneurons. Eur J Neurosci 5:1719–1728

    Article  PubMed  Google Scholar 

  • Sorra KE, Harris KM (1993) Occurrence and three-dimensional structure of multiple synapses between individual radiatum axons and their target pyramidal cells in hippocampal area CA1. J Neurosci 13:3736–3748

    PubMed  CAS  Google Scholar 

  • Squire LR (1992) Memory and the hippocampus–a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99:195–231

    Article  PubMed  CAS  Google Scholar 

  • Tamamaki N, Abe K, Nojyo Y (1988) Three-dimensional analysis of the whole axonal arbors originating from single CA2 pyramidal neurons in the rat hippocampus with the aid of a computer graphic technique. Brain Res 452:255–272

    Article  PubMed  CAS  Google Scholar 

  • Treves A, Rolls ET (1994) Computational analysis of the role of the hippocampus in memory. Hippocampus 4:374–391

    Article  PubMed  CAS  Google Scholar 

  • Turner DA, Li XG, Pyapali GK, Ylinen A, Buzsáki G (1995) Morphometric and electrical properties of reconstructed hippocampal CA3 neurons recorded in vivo. J Comp Neurol 356:580–594

    Article  PubMed  CAS  Google Scholar 

  • Wittner L, Henze DA, Záborszky L, Buzsáki G (2006) Hippocampal CA3 pyramidal cells selectively innervate aspiny interneurons. Eur J Neurosci 24:1286–1298

    Article  PubMed  Google Scholar 

  • Wong RK, Traub RD (1983) Synchronized burst discharge in disinhibited hippocampal slice. I. Initiation in CA2-CA3 region. J Neurophysiol 49:442–458

    PubMed  CAS  Google Scholar 

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Acknowledgments

This research was supported by NIH (MH54671 to GB and NSO23945 to LZ). We would like to thank Alvaro Duque for support and teaching the use of NeuroLucida.

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Author notes

  1. Darrell A. Henze

    Present address: Merck Research Laboratories, West Point, PA, 19486, USA

Authors and Affiliations

  1. Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey, 197 University Avenue, Newark, NJ, 07102, USA

    Lucia Wittner, Darrell A. Henze, László Záborszky & György Buzsáki

  2. Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, Hungary

    Lucia Wittner

  3. Institute for Psychology, Hungarian Academy of Sciences, Budapest, Hungary

    Lucia Wittner

Authors
  1. Lucia Wittner
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  2. Darrell A. Henze
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  3. László Záborszky
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  4. György Buzsáki
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Corresponding author

Correspondence to György Buzsáki.

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Wittner, L., Henze, D.A., Záborszky, L. et al. Three-dimensional reconstruction of the axon arbor of a CA3 pyramidal cell recorded and filled in vivo. Brain Struct Funct 212, 75–83 (2007). https://doi.org/10.1007/s00429-007-0148-y

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  • DOI: https://doi.org/10.1007/s00429-007-0148-y

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