Brain Structure and Function

, Volume 212, Issue 1, pp 75–83 | Cite as

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

  • Lucia Wittner
  • Darrell A. Henze
  • László Záborszky
  • György BuzsákiEmail author
Original Article


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.


Dentate Gyrus Granule Cell Layer Axon Initial Segment Axon Collateral Biocytin 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



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.

Supplementary material

429_2007_148_MOESM1_ESM.avi (19.3 mb)
(AVI 19783 kb)


  1. Amaral DG, Witter MP (1989) The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31:571–591PubMedCrossRefGoogle Scholar
  2. Andersen P, Bliss TV, Lomo T, Olsen LI, Skrede KK (1969) Lamellar organization of hippocampal excitatory pathways. Acta Physiol Scand 76:4A–5APubMedGoogle Scholar
  3. Andersen P, Soleng AF, Raastad M (2000) The hippocampal lamella hypothesis revisited. Brain Res 886:165–171PubMedCrossRefGoogle Scholar
  4. 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 366:271–292PubMedCrossRefGoogle Scholar
  5. Buhl DL, Buzsáki G (2005) Developmental emergence of hippocampal fast-field “ripple” oscillations in the behaving rat pups. Neuroscience 134:1423–1430PubMedCrossRefGoogle Scholar
  6. Buzsáki G (1986) Hippocampal sharp waves: their origin and significance. Brain Res 398:242–252PubMedCrossRefGoogle Scholar
  7. Buzsáki G, Leung LW, Vanderwolf CH (1983) Cellular bases of hippocampal EEG in the behaving rat. Brain Res 287:139–171PubMedGoogle Scholar
  8. Buzsáki G, Horvath Z, Urioste R, Hetke J, Wise K (1992) High-frequency network oscillation in the hippocampus. Science 256:1025–1027PubMedCrossRefGoogle Scholar
  9. Csicsvári J, Jamieson B, Wise KD, Buzsáki G (2003) Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37:311–322PubMedCrossRefGoogle Scholar
  10. 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 271:201–216PubMedCrossRefGoogle Scholar
  11. Grossman Y, Parnas I, Spira ME (1979) Differential conduction block in branches of a bifurcating axon. J Physiol 295:283–305PubMedGoogle Scholar
  12. Hampson RE, Simeral JD, Deadwyler SA (1999) Distribution of spatial and nonspatial information in dorsal hippocampus. Nature 402:610–614PubMedCrossRefGoogle Scholar
  13. 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 14:793–817PubMedCrossRefGoogle Scholar
  14. Ishizuka N, Weber J, Amaral DG (1990) Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J Comp Neurol 295:580–623PubMedCrossRefGoogle Scholar
  15. Jefferys JG (1995) Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions. Physiol Rev 75:689–723PubMedGoogle Scholar
  16. Kanerva P (1988) Sparse distributed memory. The MIT Press, CambridgeGoogle Scholar
  17. 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 451:33–42PubMedCrossRefGoogle Scholar
  18. Li XG, Somogyi P, Ylinen A, Buzsáki G (1994) The hippocampal CA3 network: an in vivo intracellular labeling study. J Comp Neurol 339:181–208PubMedCrossRefGoogle Scholar
  19. Lőrincz A, Buzsáki G (2000) Two-phase computational model training long-term memories in the entorhinal-hippocampal region. Ann N Y Acad Sci 911:83–111PubMedCrossRefGoogle Scholar
  20. Luscher HR, Shiner JS (1990a) Computation of action potential propagation and presynaptic bouton activation in terminal arborizations of different geometries. Biophys J 58:1377–1388PubMedCrossRefGoogle Scholar
  21. Luscher HR, Shiner JS (1990b) Simulation of action potential propagation in complex terminal arborizations. Biophys J 58:1389–1399PubMedGoogle Scholar
  22. Martin SJ, Clark RE (2007) The rodent hippocampus and spatial memory: from synapses to systems. Cell Mol Life Sci 64:401–431PubMedCrossRefGoogle Scholar
  23. McNaughton BL, Morris RGM (1987) Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 10:408–415CrossRefGoogle Scholar
  24. McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser MB (2006) Path integration and the neural basis of the ‘cognitive map’. Nat Rev Neurosci 7:663–678PubMedCrossRefGoogle Scholar
  25. Miles R, Wong RK (1983) Single neurones can initiate synchronized population discharge in the hippocampus. Nature 306:371–373PubMedCrossRefGoogle Scholar
  26. Muller RU, Stead M, Pach J (1996) The hippocampus as a cognitive graph. J Gen Physiol 107:663–694PubMedCrossRefGoogle Scholar
  27. Paxinos G, Watson C (1982) The rat brain in stereotaxic coordinates. Academic, SidneyGoogle Scholar
  28. Redish AD, Rosenzweig ES, Bohanick JD, McNaughton BL, Barnes CA (2000) Dynamics of hippocampal ensemble activity realignment: time versus space. J Neurosci 20:9298–9309PubMedGoogle Scholar
  29. 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 18:8300–8310PubMedGoogle Scholar
  30. 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 5:1719–1728PubMedCrossRefGoogle Scholar
  31. 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 13:3736–3748PubMedGoogle Scholar
  32. Squire LR (1992) Memory and the hippocampus–a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99:195–231PubMedCrossRefGoogle Scholar
  33. 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 452:255–272PubMedCrossRefGoogle Scholar
  34. Treves A, Rolls ET (1994) Computational analysis of the role of the hippocampus in memory. Hippocampus 4:374–391PubMedCrossRefGoogle Scholar
  35. 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 356:580–594PubMedCrossRefGoogle Scholar
  36. Wittner L, Henze DA, Záborszky L, Buzsáki G (2006) Hippocampal CA3 pyramidal cells selectively innervate aspiny interneurons. Eur J Neurosci 24:1286–1298PubMedCrossRefGoogle Scholar
  37. Wong RK, Traub RD (1983) Synchronized burst discharge in disinhibited hippocampal slice. I. Initiation in CA2-CA3 region. J Neurophysiol 49:442–458PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Lucia Wittner
    • 1
    • 2
    • 3
  • Darrell A. Henze
    • 1
    • 4
  • László Záborszky
    • 1
  • György Buzsáki
    • 1
    Email author
  1. 1.Center for Molecular and Behavioral NeuroscienceRutgers, The State University of New JerseyNewarkUSA
  2. 2.Institute of Experimental MedicineHungarian Academy of SciencesBudapestHungary
  3. 3.Institute for PsychologyHungarian Academy of SciencesBudapestHungary
  4. 4.Merck Research LaboratoriesWest PointUSA

Personalised recommendations