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Erschienen in: Brain Structure and Function 1/2007

01.07.2007 | Original Article

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

verfasst von: Lucia Wittner, Darrell A. Henze, László Záborszky, György Buzsáki

Erschienen in: Brain Structure and Function | Ausgabe 1/2007

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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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Literatur
Zurück zum Zitat Amaral DG, Witter MP (1989) The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31:571–591PubMedCrossRef Amaral DG, Witter MP (1989) The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31:571–591PubMedCrossRef
Zurück zum Zitat Andersen P, Bliss TV, Lomo T, Olsen LI, Skrede KK (1969) Lamellar organization of hippocampal excitatory pathways. Acta Physiol Scand 76:4A–5APubMed Andersen P, Bliss TV, Lomo T, Olsen LI, Skrede KK (1969) Lamellar organization of hippocampal excitatory pathways. Acta Physiol Scand 76:4A–5APubMed
Zurück zum Zitat Andersen P, Soleng AF, Raastad M (2000) The hippocampal lamella hypothesis revisited. Brain Res 886:165–171PubMedCrossRef Andersen P, Soleng AF, Raastad M (2000) The hippocampal lamella hypothesis revisited. Brain Res 886:165–171PubMedCrossRef
Zurück zum Zitat 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 366:271–292PubMedCrossRef 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 366:271–292PubMedCrossRef
Zurück zum Zitat Buhl DL, Buzsáki G (2005) Developmental emergence of hippocampal fast-field “ripple” oscillations in the behaving rat pups. Neuroscience 134:1423–1430PubMedCrossRef Buhl DL, Buzsáki G (2005) Developmental emergence of hippocampal fast-field “ripple” oscillations in the behaving rat pups. Neuroscience 134:1423–1430PubMedCrossRef
Zurück zum Zitat Buzsáki G (1986) Hippocampal sharp waves: their origin and significance. Brain Res 398:242–252PubMedCrossRef Buzsáki G (1986) Hippocampal sharp waves: their origin and significance. Brain Res 398:242–252PubMedCrossRef
Zurück zum Zitat Buzsáki G, Leung LW, Vanderwolf CH (1983) Cellular bases of hippocampal EEG in the behaving rat. Brain Res 287:139–171PubMed Buzsáki G, Leung LW, Vanderwolf CH (1983) Cellular bases of hippocampal EEG in the behaving rat. Brain Res 287:139–171PubMed
Zurück zum Zitat Buzsáki G, Horvath Z, Urioste R, Hetke J, Wise K (1992) High-frequency network oscillation in the hippocampus. Science 256:1025–1027PubMedCrossRef Buzsáki G, Horvath Z, Urioste R, Hetke J, Wise K (1992) High-frequency network oscillation in the hippocampus. Science 256:1025–1027PubMedCrossRef
Zurück zum Zitat Csicsvári J, Jamieson B, Wise KD, Buzsáki G (2003) Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37:311–322PubMedCrossRef Csicsvári J, Jamieson B, Wise KD, Buzsáki G (2003) Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37:311–322PubMedCrossRef
Zurück zum Zitat 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 271:201–216PubMedCrossRef 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 271:201–216PubMedCrossRef
Zurück zum Zitat Grossman Y, Parnas I, Spira ME (1979) Differential conduction block in branches of a bifurcating axon. J Physiol 295:283–305PubMed Grossman Y, Parnas I, Spira ME (1979) Differential conduction block in branches of a bifurcating axon. J Physiol 295:283–305PubMed
Zurück zum Zitat Hampson RE, Simeral JD, Deadwyler SA (1999) Distribution of spatial and nonspatial information in dorsal hippocampus. Nature 402:610–614PubMedCrossRef Hampson RE, Simeral JD, Deadwyler SA (1999) Distribution of spatial and nonspatial information in dorsal hippocampus. Nature 402:610–614PubMedCrossRef
Zurück zum Zitat 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 14:793–817PubMedCrossRef 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 14:793–817PubMedCrossRef
Zurück zum Zitat Ishizuka N, Weber J, Amaral DG (1990) Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J Comp Neurol 295:580–623PubMedCrossRef Ishizuka N, Weber J, Amaral DG (1990) Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J Comp Neurol 295:580–623PubMedCrossRef
Zurück zum Zitat Jefferys JG (1995) Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions. Physiol Rev 75:689–723PubMed Jefferys JG (1995) Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions. Physiol Rev 75:689–723PubMed
Zurück zum Zitat Kanerva P (1988) Sparse distributed memory. The MIT Press, Cambridge Kanerva P (1988) Sparse distributed memory. The MIT Press, Cambridge
Zurück zum Zitat 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 451:33–42PubMedCrossRef 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 451:33–42PubMedCrossRef
Zurück zum Zitat Li XG, Somogyi P, Ylinen A, Buzsáki G (1994) The hippocampal CA3 network: an in vivo intracellular labeling study. J Comp Neurol 339:181–208PubMedCrossRef Li XG, Somogyi P, Ylinen A, Buzsáki G (1994) The hippocampal CA3 network: an in vivo intracellular labeling study. J Comp Neurol 339:181–208PubMedCrossRef
Zurück zum Zitat Lőrincz A, Buzsáki G (2000) Two-phase computational model training long-term memories in the entorhinal-hippocampal region. Ann N Y Acad Sci 911:83–111PubMedCrossRef Lőrincz A, Buzsáki G (2000) Two-phase computational model training long-term memories in the entorhinal-hippocampal region. Ann N Y Acad Sci 911:83–111PubMedCrossRef
Zurück zum Zitat Luscher HR, Shiner JS (1990a) Computation of action potential propagation and presynaptic bouton activation in terminal arborizations of different geometries. Biophys J 58:1377–1388PubMedCrossRef Luscher HR, Shiner JS (1990a) Computation of action potential propagation and presynaptic bouton activation in terminal arborizations of different geometries. Biophys J 58:1377–1388PubMedCrossRef
Zurück zum Zitat Luscher HR, Shiner JS (1990b) Simulation of action potential propagation in complex terminal arborizations. Biophys J 58:1389–1399PubMed Luscher HR, Shiner JS (1990b) Simulation of action potential propagation in complex terminal arborizations. Biophys J 58:1389–1399PubMed
Zurück zum Zitat Martin SJ, Clark RE (2007) The rodent hippocampus and spatial memory: from synapses to systems. Cell Mol Life Sci 64:401–431PubMedCrossRef Martin SJ, Clark RE (2007) The rodent hippocampus and spatial memory: from synapses to systems. Cell Mol Life Sci 64:401–431PubMedCrossRef
Zurück zum Zitat McNaughton BL, Morris RGM (1987) Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 10:408–415CrossRef McNaughton BL, Morris RGM (1987) Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 10:408–415CrossRef
Zurück zum Zitat McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser MB (2006) Path integration and the neural basis of the ‘cognitive map’. Nat Rev Neurosci 7:663–678PubMedCrossRef McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser MB (2006) Path integration and the neural basis of the ‘cognitive map’. Nat Rev Neurosci 7:663–678PubMedCrossRef
Zurück zum Zitat Miles R, Wong RK (1983) Single neurones can initiate synchronized population discharge in the hippocampus. Nature 306:371–373PubMedCrossRef Miles R, Wong RK (1983) Single neurones can initiate synchronized population discharge in the hippocampus. Nature 306:371–373PubMedCrossRef
Zurück zum Zitat Muller RU, Stead M, Pach J (1996) The hippocampus as a cognitive graph. J Gen Physiol 107:663–694PubMedCrossRef Muller RU, Stead M, Pach J (1996) The hippocampus as a cognitive graph. J Gen Physiol 107:663–694PubMedCrossRef
Zurück zum Zitat Paxinos G, Watson C (1982) The rat brain in stereotaxic coordinates. Academic, Sidney Paxinos G, Watson C (1982) The rat brain in stereotaxic coordinates. Academic, Sidney
Zurück zum Zitat Redish AD, Rosenzweig ES, Bohanick JD, McNaughton BL, Barnes CA (2000) Dynamics of hippocampal ensemble activity realignment: time versus space. J Neurosci 20:9298–9309PubMed Redish AD, Rosenzweig ES, Bohanick JD, McNaughton BL, Barnes CA (2000) Dynamics of hippocampal ensemble activity realignment: time versus space. J Neurosci 20:9298–9309PubMed
Zurück zum Zitat 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 18:8300–8310PubMed 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 18:8300–8310PubMed
Zurück zum Zitat 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 5:1719–1728PubMedCrossRef 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 5:1719–1728PubMedCrossRef
Zurück zum Zitat 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 13:3736–3748PubMed 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 13:3736–3748PubMed
Zurück zum Zitat Squire LR (1992) Memory and the hippocampus–a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99:195–231PubMedCrossRef Squire LR (1992) Memory and the hippocampus–a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99:195–231PubMedCrossRef
Zurück zum Zitat 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 452:255–272PubMedCrossRef 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 452:255–272PubMedCrossRef
Zurück zum Zitat Treves A, Rolls ET (1994) Computational analysis of the role of the hippocampus in memory. Hippocampus 4:374–391PubMedCrossRef Treves A, Rolls ET (1994) Computational analysis of the role of the hippocampus in memory. Hippocampus 4:374–391PubMedCrossRef
Zurück zum Zitat 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 356:580–594PubMedCrossRef 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 356:580–594PubMedCrossRef
Zurück zum Zitat Wittner L, Henze DA, Záborszky L, Buzsáki G (2006) Hippocampal CA3 pyramidal cells selectively innervate aspiny interneurons. Eur J Neurosci 24:1286–1298PubMedCrossRef Wittner L, Henze DA, Záborszky L, Buzsáki G (2006) Hippocampal CA3 pyramidal cells selectively innervate aspiny interneurons. Eur J Neurosci 24:1286–1298PubMedCrossRef
Zurück zum Zitat Wong RK, Traub RD (1983) Synchronized burst discharge in disinhibited hippocampal slice. I. Initiation in CA2-CA3 region. J Neurophysiol 49:442–458PubMed Wong RK, Traub RD (1983) Synchronized burst discharge in disinhibited hippocampal slice. I. Initiation in CA2-CA3 region. J Neurophysiol 49:442–458PubMed
Metadaten
Titel
Three-dimensional reconstruction of the axon arbor of a CA3 pyramidal cell recorded and filled in vivo
verfasst von
Lucia Wittner
Darrell A. Henze
László Záborszky
György Buzsáki
Publikationsdatum
01.07.2007
Verlag
Springer-Verlag
Erschienen in
Brain Structure and Function / Ausgabe 1/2007
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-007-0148-y

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