Skip to main content

Advertisement

Log in

Successes and Rewards in Sharing Digital Reconstructions of Neuronal Morphology

  • Published:
Neuroinformatics Aims and scope Submit manuscript

Abstract

The computer-assisted three-dimensional reconstruction of neuronal morphology is becoming an increasingly popular technique to quantify the arborization patterns of dendrites and axons. The resulting digital files are suitable for comprehensive morphometric analyses as well as for building anatomically realistic compartmental models of membrane biophysics and neuronal electrophysiology. The digital tracings acquired in a lab for a specific purpose can be often re-used by a different research group to address a completely unrelated scientific question, if the original investigators are willing to share the data. Since reconstructing neuronal morphology is a labor-intensive process, data sharing and re-analysis is particularly advantageous for the neuroscience and biomedical communities. Here we present numerous cases of “success stories” in which digital reconstructions of neuronal morphology were shared and re-used, leading to additional, independent discoveries and publications, and thus amplifying the impact of the “source” study for which the data set was first collected. In particular, we overview four main applications of this kind of data: comparative morphometric analyses, statistical estimation of potential synaptic connectivity, morphologically accurate electrophysiological simulations, and computational models of neuronal shape and development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ambros-Ingerson, J., & Holmes, W. R. (2005). Analysis and comparison of morphological reconstructions of hippocampal field CA1 pyramidal cells. Hippocampus, 15, 302–315.

    Article  PubMed  Google Scholar 

  • Ascoli, G. A. (2002). Neuroanatomical algorithms for dendritic modeling. Network: Computation in Neural Systems, 13, 247–260.

    Article  Google Scholar 

  • Ascoli, G. A. (2006). Mobilizing the base of neuroscience data: the case of neuronal morphologies. Nature Reviews Neuroscience, 7, 318–324.

    Article  PubMed  CAS  Google Scholar 

  • Ascoli, G. A., Krichmar, J. L., Scorcioni, R., Nasuto, S., & Senft, S. L. (2001). Computer generation and quantitative morphometric analysis of virtual neurons. Anatomy Embryology, 204, 283–301.

    Article  CAS  Google Scholar 

  • Bannister, N. J., & Larkman, A. U. (1995). Dendritic morphology of CA1 pyramidal neurones from the rat hippocampus. I. Branching patterns. Journal of Comparative Neurology, 360, 150–160.

    Article  PubMed  CAS  Google Scholar 

  • Burke, R. E., Marks, W. B., & Ulfhake, B. (1992). A parsimonious description of motoneuron dendritic morphology using computer simulation. Journal of Neuroscience, 12, 2403–2416.

    PubMed  CAS  Google Scholar 

  • Cannon, R. C., Wheal, H. V., & Turner, D. A. (1999). Dendrites of classes of hippocampal neurons differ in structural complexity and branching patterns. Journal of Comparative Neurology, 413, 619–633.

    Article  PubMed  CAS  Google Scholar 

  • Carnevale, N. T., Tsai, K. Y., Claiborne, B. J., & Brown, T. H. (1997). Comparative electrotonic analysis of three classes of rat hippocampal neurons. Journal of Neurophysiology, 78, 703–720.

    PubMed  CAS  Google Scholar 

  • Chklovskii, D. B. (2004). Synaptic connectivity and neuronal morphology: Two sides of the same coin. Neuron, 43, 609–617.

    PubMed  CAS  Google Scholar 

  • Costa, L. F., & Manoel, E. T. M. (2003). A percolation approach to neural morphometry and connectivity. Neuroinformatics, 1, 65–80.

    Article  Google Scholar 

  • Costa, L. F., & Velte, T. J. (1999). Automatic characterization and classification of ganglion cells from the salamander retina. Journal of Comparative Neurology, 404, 33–51.

    Article  Google Scholar 

  • Crook, S., Gleeson, P., Howell, F., Svitak, J., & Silver, R. A. (2007). MorphML: Level 1 of the NeuroML standards for neuronal morphology data and model specification. Neuroinformatics (in press).

  • Cullheim, S., Fleshman, J. W., Glenn, L. L., & Burke, R. E. (1987). Membrane area and dendritic structure in type-identified triceps surae alphamotoneurons. Journal of Comparative Neurology, 255, 68–81.

    Article  PubMed  CAS  Google Scholar 

  • De Schutter, E., & Bower, J. M. (1994). An active membrane model of the cerebellar Purkinje cell. Journal of Neurophysiology, 71, 375–419.

    PubMed  Google Scholar 

  • Donohue, D., & Ascoli, G. A. (2005a). Models of neuronal outgrowth. In: S. H. Koslow, & Subramaniam, S. (Eds). Databasing the brain: From data to knowledge New York, NY: Wiley.

    Google Scholar 

  • Donohue, D. E., & Ascoli, G. A. (2005b). Local diameter fully constrains dendritic size in basal but not apical trees of CA1 pyramidal neurons. Journal of Computational Neuroscience, 19, 223–238.

    Article  PubMed  Google Scholar 

  • Duan, H. L., Wearne, S. L., Rocher, A. B., Macedo, A., Morrison, J. H., & Hof, P. R. (2003). Age-related dendritic andspine changes in corticocortically projecting neurons in macaque monkeys. Cerebral Cortex, 13, 950–961.

    Article  PubMed  Google Scholar 

  • Eckersley, P., et al. (2003). Neuroscience data and tool sharing: A legal and policy framework for neuroinformatics. Neuroinformatics, 1, 149–165.

    Article  PubMed  Google Scholar 

  • Fohlmeister, J. F., & Miller, R. F. (1997). Impulse encoding mechanisms of ganglion cells in the tiger salamander retina. Journal of Neurophysiology, 78, 1935–1947.

    PubMed  CAS  Google Scholar 

  • Gardner, D., et al. (2003). Towards effective and rewarding data sharing. Neuroinformatics, 1, 289–295.

    Article  PubMed  Google Scholar 

  • Geschwind, D. H. (2001). Sharing gene expression data: an array of options. Nature Reviews Neuroscience, 2, 435–438.

    Article  PubMed  CAS  Google Scholar 

  • Henze, D. A., Cameron, W. E., & Barrionuevo, G. (1996). Dendritic morphology and its effects on the amplitude and rise-time of synaptic signals in hippocampal CA3 pyramidal cells. Journal of Comparative Neurology, 369, 331–344.

    Article  PubMed  CAS  Google Scholar 

  • Holmes, W. R., Ambros-Ingerson, J., & Grover, L. M. (2006). Fitting experimental data to models that use morphological data from public databases. Journal of Computational Neuroscience, 20, 349–365.

    Article  PubMed  CAS  Google Scholar 

  • Insel, T. R., Volkow, N. D., Li, T. K., Battey, J. F., & Landis, S. C. (2003). Neuroscience networks: Data-sharing in an information age. PLoS Biology, 1, e17.

    Article  Google Scholar 

  • Ishizuka, N., Cowan, W. M., & Amaral, D. G. (1995). A quantitative analysis of the dendritic organization of pyramidal cells in the rat hippocampus. Journal Comparative Neurology, 362, 17–45.

    Article  PubMed  CAS  Google Scholar 

  • Jacobs, G. A., & Theunissen, F. (1996). Functional organization of a neural map in the cricket cercal sensory system. Journal of Neuroscience, 16, 769–784.

    PubMed  CAS  Google Scholar 

  • Jaeger, D. (2000). Accurate reconstruction of neuronal morphology. In: E. De Schutter (Ed.), Computational neuroscience: Realistic modeling for experimentalists (pp. 159–178). Boca Raton, FL: CRC.

    Google Scholar 

  • Jefferis, G. S. X. E., Potter, C. J., Chan, A. M., Marin, E. C., Rohlfing, T., Maurer, C. R., et al. (2007). Comprehensive maps of Drosophila higher olfactory centers: Spatially segregated fruit and pheromone representation. Cell, 128, 1187–1203.

    Article  PubMed  CAS  Google Scholar 

  • Kalisman, N., Silberberg, G., & Markram, H. (2003). Deriving physical connectivity from neuronal morphology. Biological Cybernetics, 88, 210–218.

    Article  PubMed  Google Scholar 

  • Koslow, S. H. (2000). Should the neuroscience community make a paradigm shift to sharing primary data?. Nature Neuroscience, 3, 863–865.

    Article  PubMed  CAS  Google Scholar 

  • Koslow, S. H. (2002). Sharing primary data: A threat or asset to discovery? Nature Reviews Neuroscience, 3, 311–313.

    Article  PubMed  CAS  Google Scholar 

  • Krichmar, J. L., Nasuto, S., Scorcioni, R., Washington, S., & Ascoli, G. A. (2002). Effects of dendritic morphology on CA3 pyramidal cell electrophysiology: a simulation study. Brain Research, 941, 11–28.

    Article  PubMed  CAS  Google Scholar 

  • Li, X., & Ascoli, G. A. (2006). Computational simulation of the input–output relationship in hippocampal pyramidal cells. Journal of Computational Neuroscience, 21, 191–209.

    Article  PubMed  Google Scholar 

  • Lindsay, K. A., Maxwell, D. J., Rosenberg, J. R., & Tucker, G. (2007). A new approach to reconstruction models of dendritic branching patterns. Mathematical Bioscience, 205, 271–296.

    Article  Google Scholar 

  • Luczak, A. (2006). Spatial embedding of neuronal trees modeled by diffusive growth. Journal of Neuroscience Methods, 157, 132–141.

    Article  PubMed  Google Scholar 

  • Mainen, Z. F., & Sejnowski, T. (1996). Influence of dendritic structure on firing pattern in model neocortical neurons. Nature, 382, 363–366.

    Article  PubMed  CAS  Google Scholar 

  • Marks, W. B., & Burke R. E. (2007). Simulation of motoneuron morphology in three dimensions. Journal of Comparative Neurology, 503, 685–716.

    Article  PubMed  Google Scholar 

  • Megias, M., Emri, Z., Freund, T. F., & Gulyas, A. I. (2001). Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience, 102, 527–540.

    Article  PubMed  CAS  Google Scholar 

  • Migliore, M., Ferrante, M., & Ascoli, G. A. (2005). Signal propagation in oblique dendrites of CA1 pyramidal cells. Journal of Neurophysiology, 94:4145–4155.

    Article  PubMed  Google Scholar 

  • Mott, D. D., Turner, D. A., Okazaki, M. M., & Lewis, D. V. (1997). Interneurons of the dentate-hilus border of the rat dentate gyrus: Morphological and electrophysiological heterogeneity. Journal of Neuroscience, 17, 3990–4005.

    PubMed  CAS  Google Scholar 

  • Olave, M. J., Puri, N., Kerr, R., & Maxwell, D. J. (2002). Myelinated and unmyelinated primary afferent axons form contacts with cholinergic interneurons in the spinal dorsal horn. Experimental Brain Research, 145, 448–456.

    Article  CAS  Google Scholar 

  • Piwowar, H. A., Day, R. S., & Fridsma, D. B. (2007). Sharing detailed research data is associated with increased citation rate. PLoS One, 2(3), e308.

    Article  PubMed  Google Scholar 

  • Pyapali, G. K., Sik, A., Penttonen, M., Buzsaki, G., & Turner, D. A. (1998). Dendritic properties of hippocampal CA1 pyramidal neurons in the rat: Intracellular staining in vivo and in vitro. Journal of Comparative Neurology, 391, 335–352.

    Article  PubMed  CAS  Google Scholar 

  • Pyapali, G. K., & Turner, D. A. (1994). Denervation-induced dendritic alterations in CA1 pyramidal cells following kainic acid hippocampal lesions in rats. Brain Research, 652, 279–290.

    Article  PubMed  CAS  Google Scholar 

  • Pyapali, G. K., & Turner, D. A. (1996). Increased dendritic extent in hippocampal CA1 neurons from aged F344 rats. Neurobiology of Aging, 17, 601–611.

    Article  PubMed  CAS  Google Scholar 

  • Rapp, M., Segev, I., & Yarom, Y. (1994). Physiology, morphology, and detailed passive models of guinea-pig cerebellar Purkinje cells. Journal of Physiology, 474, 101–108.

    PubMed  CAS  Google Scholar 

  • Rihn, L. L., & Claiborne, B. J. (1990). Dendritic growth and regression in rat dentate granule cells during late postnatal development. Brain Research, Developmental Brain Research, 54, 115–124.

    Article  CAS  Google Scholar 

  • Samsonovich, A. V., & Ascoli, G. A. (2003). Statistical morphological analysis of hippocampal principal neurons indicates selective repulsion of dendrites from their own cell. Journal of Neuroscience Research, 71, 173–187.

    Article  PubMed  CAS  Google Scholar 

  • Samsonovich, A. V., & Ascoli, G. A. (2005a). Statistical determinants of dendritic morphology in hippocampal pyramidal neurons: A hidden Markov model. Hippocampus, 15, 166–183.

    Article  PubMed  Google Scholar 

  • Samsonovich, A. V., & Ascoli, G. A. (2005b). Algorithmic description of hippocampal granule cell dendritic morphology. Neurocomputing, 65–66, 253–260.

    Article  Google Scholar 

  • Samsonovich, A. V., & Ascoli, G. A. (2006). Morphological homeostasis in cortical dendrites. PNAS, 103, 1569–1574.

    Article  PubMed  CAS  Google Scholar 

  • Schaefer, A. T., Larkum, M. E., Sakmann, B., & Roth, A. (2003). Coincidence detection in pyramidal neurons is tuned by their dendritic branching pattern. Journal of Neurophysiology, 89, 3143–3154.

    Article  PubMed  Google Scholar 

  • Scorcioni, R., Bouteiller, J., & Ascoli, G. A. (2002). A real-scale anatomical model of the dentate gyrus based on single cell reconstructions and 3D rendering of a brain atlas. Neurocomputing, 44–46, 629–634.

    Article  Google Scholar 

  • Scorcioni, R., Lazarewicz, M., & Ascoli, G. A. (2004). Quantitative morphometry of hippocampal pyramidal cells: Differences between anatomical classes and reconstructing laboratories. Journal of Comparative Neurology, 473, 177–193.

    Article  PubMed  Google Scholar 

  • Shepherd, G. M., Stepanyants, A., Bureau, I., Chklovskii, D., & Svoboda, K. (2005). Geometric and functional organization of cortical circuits. Nature Neuroscience, 8, 782–790.

    Article  PubMed  CAS  Google Scholar 

  • Stepanyants, A., & Chklovskii, D. B. (2005). Neurogeometry and potential synaptic connectivity. Trends in Neurosciences, 28, 387–394.

    Article  PubMed  CAS  Google Scholar 

  • Stepanyants, A., Hirsch, J. A., Martinez, L. M., Kisvarday, Z. F., Ferecsko, A. S., & Chklovskii, D. B. (2007). Local potential connectivity in cat primary visual cortex. Cerebral Cortex (in press).

  • Stepanyants, A., Hof, P. R., & Chklovskii, D. B. (2002). Geometry and structural plasticity of synaptic connectivity. Neuron, 34, 275–288.

    Article  PubMed  CAS  Google Scholar 

  • Stepanyants, A., Tamas, G., & Chklovskii, D. B. (2004). Class-specific features of neuronal wiring. Neuron, 43, 251–259.

    Article  PubMed  CAS  Google Scholar 

  • Szilagyi, T., De Schutter, E. (2004). Effects of variability in anatomical reconstruction techniques on models of synaptic integration by dendrites: A comparison of three Internet archives. European Journal of Neuroscience, 19, 1257–1266.

    Article  PubMed  Google Scholar 

  • Toris, C. B., Eiesland, J. L., & Miller, R. F. (1995). Morphology of ganglion cells in the neotenous tiger salamander retina. Journal of Comparative Neurology, 352, 535–559.

    Article  PubMed  CAS  Google Scholar 

  • Turner, D. A., Li, X. G., Pyapali, G. K., Ylinen, A., & Buzsaki, G. (1995). Morphometric and electrical properties of reconstructed hippocampal CA3 neurons recorded in vivo. Journal of Comparative Neurology, 356, 580–594.

    Article  PubMed  CAS  Google Scholar 

  • Van Ooyen, A., Van Pelt, J. (2002). Competition in neuronal morphogenesis and the development of nerve connections. In: Ascoli, G. A, (Ed.), Computational neuroanatomy: Principles and methods. Totowa, NJ: Humana.

    Google Scholar 

  • Vetter, P., Roth, A., & Hausser, M. (2001). Propagation of action potentials in dendrites depends on dendritic morphology. Journal of Neurophysiology, 85, 926–937.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by NIH grants NS39600, AG025633, and DA-HHSN271200577531C.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Giorgio A. Ascoli.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ascoli, G.A. Successes and Rewards in Sharing Digital Reconstructions of Neuronal Morphology. Neuroinform 5, 154–160 (2007). https://doi.org/10.1007/s12021-007-0010-7

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12021-007-0010-7

Keywords

Navigation