Morphometric and electrical properties of reconstructed hippocampal CA3 neurons recorded in vivo
Corresponding Author
D. A. Turner
Departments of Neurosurgery Durham, North Carolina 27710
Departments of Neurosurgery and Neurobiology, Durham, North Carolina 27710
Duke University Medical Center, and Durham Veterans Administration Medical Center, Durham, North Carolina 27710
MA, MD, Box 3807, Neurosurgery, Duke University Medical Center, Durham, NC 27710Search for more papers by this authorX.-G. Li
Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey, Newark, New Jersey 07102
Search for more papers by this authorG. K. Pyapali
Departments of Neurosurgery Durham, North Carolina 27710
Search for more papers by this authorDr. A. Ylinen
Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey, Newark, New Jersey 07102
Search for more papers by this authorG. Buzsaki
Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey, Newark, New Jersey 07102
Search for more papers by this authorCorresponding Author
D. A. Turner
Departments of Neurosurgery Durham, North Carolina 27710
Departments of Neurosurgery and Neurobiology, Durham, North Carolina 27710
Duke University Medical Center, and Durham Veterans Administration Medical Center, Durham, North Carolina 27710
MA, MD, Box 3807, Neurosurgery, Duke University Medical Center, Durham, NC 27710Search for more papers by this authorX.-G. Li
Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey, Newark, New Jersey 07102
Search for more papers by this authorG. K. Pyapali
Departments of Neurosurgery Durham, North Carolina 27710
Search for more papers by this authorDr. A. Ylinen
Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey, Newark, New Jersey 07102
Search for more papers by this authorG. Buzsaki
Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey, Newark, New Jersey 07102
Search for more papers by this authorAbstract
CA3 pyramidal neurons were stained with biocytin during intracellular recording in rat hippocampus in vivo and reconstructed using a computer-based system. The in vivo CA3 neurons were characterized primarily according to their proximity to the hilus and secondarily with respect to the septotemporal location. Neurons measured in CA3a (n = 4), in CA3b (n = 4), and in posterior/ventral locations (n = 3) had the greatest dendritic lengths (19.8, 19.1, and 26.8 mm on average, respectively). Cells closer to the hilus showed much shorter dendritic lengths, averaging 10.4 mm for CA3c neurons (n = 4) and 11.6 mm for zone 3 neurons (n = 2). Half of the cells showed more than one major apical dendrite, and dendritic trees were highly variable even within CA3 subregions. The mean electrotonic length for these cell groups averaged between 0.30 λ (CA3c) and 0.45 λ (posterior /ventral), assuming a constant specificmembrane resistivity of 60 KΩ-CM2. These CA3 neurons form a database of reconstructed neurons for further morphometric and electrical modelling studies. The large degree of variability between individual CA3 neurons indicates that both dendritic and electrical properties should be specifically calculated for each cell rather than assuming a “typical” morphology. © 1995 Wiley-Liss, Inc.
Literature Cited
- Amaral, D. G. (1978) A Golgi study of cell types in the hilar region of the hippocampus in the rat. J. Comp. Neurol. 182: 851–914.
- Amaral, D. G., and M. P. Witter (1989) The three-dimensional organization of the hippocampal formation: A review of anatomical data. Neuroscience 31: 571–591.
- Bindu, P. N., and T. Desiraju (1990) Increase of dendritic branching of CA3 neurons of hippocampus and self-stimulation areas in subjects experiencing self-stimulation of lateral hypothalamus and substantia nigraventral tegumental area. Brain Res. 171: 171–175.
- Brown, T. H., R. A., Fricke, and D. H. Perkel (1981) Passive electrical constants in three classes of hippocampal neurons. J. Neurophysiol. 46: 812–827.
- Capowski, J. J. (1989) Computer Techniques in Neuroanatomy. New York: Plenum Press.
-
Claiborne, B. J.,
A. M., Zabor,
Z. F. Mainen, and
T. H. Brown
(1992)
Computational models of hippocampal neurons.
In T. McKenna,
J. Davis, and
S. F. Zornetzer (eds):
Single Neuron Computation.
New York:
Academic Press, Inc.,
pp. 61–80.
10.1016/B978-0-12-484815-3.50009-8 Google Scholar
- Desmond, N. L., and W. B. Levy (1982) A quantitative anatomical study of the granule cell dentate fields of the rat dentate gyrus using a novel probabilistic method. J. Comp. Neurol. 212: 131–145.
- Finch, D. M., N. L., Nowlin, and T. L. Babb (1983) Demonstration of axonal projection of neurons in the rat hippocampus and subiculum by intracellular injection of HRP. Brain Res. 271: 201–216.
- Fitch, J. M., J. M., Juraska, and L. W. Washington (1989) The dendritic morphology of pyramidal neurons in the rat CA3 area. I. Cell types. Brain Res. 479: 105–114.
- Johnston, D. (1981) Passive cable properties of hippocampal CA3 pyramidal neurons. Cell. Mol. Neurobiol. 1: 41–55.
- Juraska, J. M., J. M., Fitch, and D. L. Washburne (1989) The dendritic morphology of pyramidal neurons in the rat hippocampal CA3 area. II. Effects of gender and the environment. Brain Res. 479: 115–119.
- Kita, M. A., and W. E. Armstrong (1991) A biotin-containing compound N-(2-aminoethyl) biotinamide for intracellular labeling and neuronal tracing studies: Comparison with biocytin. J. Neurosci. Methods 37: 141–150.
- Larkman, A. U. (1991) Dendritic morphology of pyramidal neurons of the visual cortex of the rat: I. Branching patterns. J. Comp. Neurol. 306: 307–319.
- Li, X. -G., P., Somogyi, J. M. Tepper, and G. Buzsaki (1992) Axonal and dendritic arborization of an intracellularly labeled chandelier cell in the CAI region of the rat hippocampus. Exp. Brain Res. 90: 519–525.
- Li, X-G., G. K., Pyapali, A. Ylinen, G. Buzsaki, and D. A. Turner (1993) 3D reconstruction of intracellularly-stained CA3 cells in rat hippocampus in vivo. Soc. Neurosci. Abstr. 19: 350.
- Li, X. -G., P., Somogyi, A. Ylinen, and G. Buzsaki (1994) The hippocampal CA3 network: An in vivo intracellular labeling study. J. Comp. Neurol. 339: 181–208.
- Lorente de Nó, R. (1934) Studies of the structure of the cerebral cortex: II. Continuation of the study of the Ammonic system. J. Psychol. Neurol. 46: 113–177.
- Marr, D. (1971) Simple memory: A theory for archicortex. Proc. Trans. R. Soc. London [Biol.] 262: 23–81.
- McNaughton, B. L., and R. G. M. Morris (1987) Hippocampal synaptic enhancement and information storage within a distributed memory system. TINS 10: 408–415.
- Minkwitz, H. -G. (1976) Zur entwinklung der neuronenstruktur des hippocampus wahrend der pra-und postnatalen ontogenese der albinoratte. I. Mitteilung: Neurohistologische darstellung der entwinklung langaxomger neurone aus den regionen CA3 und CA4. J. Hirnforsh. 17: 213–231.
- Poznanski, R. R. (1988) Membrane voltage changes in passive dendritic trees: A tapering equivalent cylinder model. J. Math. Appl. Med. Biol. 5: 113–145.
- Poznanski, R. R. (1994) Electrotonic length estimates of CA3 hippocampal pyramidal neurons. Neurosci. Res. Commun. 14: 93–100.
- Pyapali, G. K., and D. A. Turner (1994) Denervation-induced dendritic alterations in CA1 pyramidal cells following kainic acid hippocampal lesions in rats. Brain Res. 652: 279–290.
- Pyapali, G. K., D. A., Turner, and R. D. Madison (1994) Fetal transplants in kainic acid-lesioned rat hippocampus: influence of postlesion delay on graft survival and integration. Restorative Neurol. Neurosci. 6: 113–126.
- Scharfman, H. E., and P. A., Schwartzkroin (1988) Electrophysiology of morphologically-identified mossy cells in the dentate hilus recorded in guinea pig hippocampal slices. J. Neurosci. 8: 3812–3821.
- Sholl, D. A. (1953). Dendritic organization in the neurons of the visual and motor cortices of the cat. J. Anat. 87: 387–406.
- Spruston, N., and D. Johnston (1992) Perforated patch-clamp analysis of the passive membrane properties of three classes of hippocampal neurons. J. Neurophysiol. 67: 508–529.
- Spruston, N., D. B., Jaffe, S. H. Williams, and D. Johnston (1993) Voltage and space-clamp errors associated with the measurement of electrotonically remote synaptic events. J. Neurophysiol. 70: 781–802.
- Stockley, E. W., H. M., Cole, A. D. Brown, and H. V. Wheal (1993) A system for quantitative morphological measurement and electrotonic modelling of neurons: Three-dimensional reconstruction. J. Neurosci. Methods 47: 39–51.
- Tamamaki, N., K., Abe, and Y. Nojyo (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.
- Traub, R. D., and R. Miles (1991a) Multiple modes of neuronal population activity emerge after modifying specific synapses in a model of the CA3 region of the hippocampus. Ann. NY Acad. Sci. 627: 277–290.
- Traub, R. D., R. K., Wong, R. Miles, and H. Michelson (1991b) A model of a CA3 hippocampal pyramidal neurons incorporating voltage-clamp data on intrinsic conductances. J. Neurophysiol. 66: 635–650.
- Treves, A., and E. T. Rolls (1992) Computational constraints suggest the need for two distinctive input systems to the hippocampal CA3 network. Hippocampus 2: 189–200.
- Turner, D. A. (1984) Segmental cable evaluation of somatic transients inhippocampal neurons (CA1, CA3 and dentate). Biophys. J. 46: 73–84.
- Turner, D. A., and P. A. Schwartzkroin (1983) Electrical characteristics of dendrites and dendritic spines in intracellularly-stained CA3 and dentate hippocampal neurons. J. Neurosci. 3: 2381–2394.
- Turner, D. A., H. V., Wheal, E. Stockley, and H. Cole (1991) Threedimensional reconstructions and analysis of the cable properties of neurons. In J. Chad and H. Wheal (eds): Cellular Neurobiology—A Practical Approach. New York: Oxford University Press, pp. 225–246.
- Watanabe, Y., E., Gould, and B. S. McEwen (1992) Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res. 588: 341–345.