Application of the radial distribution functions for quantitative analysis of neuropil microstructure in stratum radiatum of CA1 region in hippocampus
Main Article Content
Abstract
Various structures in the brain contain important clues to the brain’s development and function. Among these, the microscopic organization of neural tissue is of particular interest since such organization directly affects the formation of local synaptic connectivity between axons and dendrites, serving as a potential factor in the brain’s development. While the organization of the brain at large and intermediate lengths had been well studied, the organization of neural tissue at scales of micrometers remains largely unknown. In particular, at present it is not known what specific structures exist in neuropil at those scales, what effect such structures have on the formation of synaptic connectivity in the brain, and what processes shape the small-scale organization of neuropil. In this work, we present an analysis of recent 3D electron microscopy reconstructions of blocks of tissue of hippocampal CA1 neuropil from rat s. radiatum to offer new insights into these questions. We propose a new statistical method for systematical analysis of the small-scale organization of neuropil, based on an adaptation of the approach of radial distribution functions from statistical physics. Our results show that the micrometer-scale organization of hippocampal CA1 neuropil can be well understood as a disordered arrangement of axonal and dendritic processes without significant small-scale coordination. We observe several deviations from this picture in the distributions of glia and dendritic spines, and discuss their significance. Finally, we shed some light on the relationship between the small-scale organization of neuropil and local synaptic connectivity.
Article Details
How to Cite
MISHCHENKO, Yuriy.
Application of the radial distribution functions for quantitative analysis of neuropil microstructure in stratum radiatum of CA1 region in hippocampus.
Medical Research Archives, [S.l.], n. 4, aug. 2016.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/604>. Date accessed: 23 nov. 2024.
Keywords
neuropil organization; neuroanatomy; electron microscopy; neurodegeneration; radial distribution function;
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Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
References
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Amaral, D.G., and Witter, M.P. (1989). The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31, 571–591.
Arbib, M.A., Erdi, P., and Szentagothai, J. (1997). Neural Organization: Structure, Function, and Dynamics (A Bradford Book).
Bonda, D.J., Bajić, V.P., Spremo-Potparevic, B., Casadesus, G., Zhu, X., Smith, M.A., and Lee, H.-G. (2010). Review: Cell cycle aberrations and neurodegeneration. Neuropathol. Appl. Neurobiol. 36, 157–163.
de Bono, M., Villu Maricq, A., Bono, M., Villu Maricq, A., de Bono, M., V., M.A., and Villu Maricq, A. (2005). Neuronal substrates of complex behaviors in C. elegans. Annu. Rev. Neurosci. 28, 451–501.
Bosking, W.H.W.W.H.W., Zhang, Y., Schofield, B., and Fitzpatrick, D. (1997). Orientation Selectivity and the Arrangement of Horizontal Connections in Tree Shrew Striate Cortex. J. Neurosci. 17, 2112.
Braitenberg, V., and Schuz, A. (1998). Cortex: statistics and geometry of neuronal connectivity. (Berlin: Springer).
Brambilla, P., Hardan, A., di Nemi, S.U., Perez, J., Soares, J.C., and Barale, F. (2003). Brain anatomy and development in autism: Review of structural MRI studies. Brain Res. Bull. 61, 557–569.
Brodmann, K., and Garey, L.J. (2005). Brodmann’s: Localisation in the Cerebral Cortex (Springer).
Cajal, R. (1909). Histologie du systeme nerveux de l’homme et des vertebres (Paris: Madrid, Instituto Ramon y Cajal).
Castellanos, F.X., Lee, P.P., Sharp, W., Jeffries, N.O., Greenstein, D.K., Clasen, L.S., Blumenthal, J.D., James, R.S., Ebens, C.L., Walter, J.M., et al. (2002). Developmental Trajectories of Brain Volume Abnormalities in Children and Adolescents With Attention-Deficit/Hyperactivity Disorder. J. Am. Med. Assoc. 288, 1740–1748.
Chandler, D. (1987). Introduction to Modern Statistical Mechanics (New York: Oxford University Press).
Chklovskii, D.B.D.B.D.B.D.B.D.B., Schikorski, T., and Stevens, C.F. (2002). Wiring optimization in cortical circuits. Neuron 34, 341–347.
Damasio, H. (2005). Human Brain Anatomy in Computerized Images (Oxford university press).
Dickson, B.J. (2002). Molecular mechanisms of axon guidance. Science (80-. ). 298, 1959–1964.
Erwin, E., Obermayer, K., and Schulten, K. (1995). Models of Orientation and Ocular Dominance Columns in the Visual Cortex: A Critical Comparison. Neural Comput. 7, 425–468.
Ferster, D., and Miller, K.D. (2000). Neural Mechanisms of Orientation Selectivity in the Visual Cortex. Annu. Rev. Neurosci. 23, 441–471.
Fiala, J.C., Kirov, S.A., Feinberq, M.D., Petrak, L.J., George, P., Goddard, C.A., and Harris, K.M. (2003). Timing of neuronal and glial ultrastructure disruption during brain slice preparation and recovery in vitro. J. Comput. Neurol. 465, 90–103.
Freeman, R.D.D. (2003). Cortical columns: a multi-parameter examination. Cereb. Cortex 13, 70.
Garrard, P., Patterson, K., Watson, P.C., and Hodges, J.R. (1998). Category specific semantic loss in dementia of Alzheimer’s type. Functional-anatomical correlations from cross-sectional analyses. Brain 121, 633–646.
Geschwind, N. (1975). The Apraxias: Neural Mechanisms of Disorders of Learned Movement. Am. Sci. 63, 188–195.
Good, C.D., Scahill, R.I., Fox, N.C., Ashburner, J., Friston, K.J., Chan, D., Crum, W.R., Rossor, M.N., and Frackowiak, R.S.J. (2002). Automatic Differentiation of Anatomical Patterns in the Human Brain: Validation with Studies of Degenerative Dementias. Neuroimage 17, 29–46.
Hamos, J.E., DeGennaro, L.J., and Drachman, D.A. (1989). Synaptic loss in Alzheimer’s disease and other dementias. Neurology 39, 355.
Harris, K.M., and Stevens, J.K. (1989). Dendritic spines of CA1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J. Neurosci. 9, 2982–2997.
Hatton, G.I. (1990). Emerging concepts of structure-function dynamics in adult brain: the hypothalamo-neurohypophysial system. Prog. Neurobiol. 34, 437–504.
Jaynes, E.T. (2003). Probability Theory: The Logic of Science. (New York: Cambridge University Press).
Kandel, E., Schwartz, J., and Jessell, T. (2000). Principles of Neural Science (McGraw-Hill Medical).
Keil, W., Schmidt, K.F., Löwel, S., and Kaschube, M. (2010). Reorganization of columnar architecture in the growing visual cortex. Proc. Natl. Acad. Sci. 107, 12293.
McLaughlin, T., and O’Leary, D.M. (2005). Molecular gradients and development of retinotopic maps. Annu. Rev. Neurosci. 28, 327–355.
McQuarrie, D.A. (2000). Statistical Mechanics (University Science Books).
Miller, K.D., Keller, J.B., and Stryker, M.P. (1989). Ocular dominance column development: analysis and simulation. Science (80-. ). 245, 605–615.
Mishchenko, Y. (2009). Automation of 3D reconstruction of neural tissue from large volume of conventional serial section transmission electron micrographs. J. Neurosci. Methods 176, 276–289.
Mishchenko, Y. (2015). A function for fast computation of large discrete Euclidean distance transforms in three or more dimensions in Matlab. Signal, Image Video Process. 9, 19.
Mishchenko, Y., and Paninski, L. (2012). Efficient methods for sampling spike trains in networks of coupled neurons. Ann. Appl. Stat. 5, 1893–1919.
Mishchenko, Y., Hu, T., Spacek, J., Mendenhall, J., Harris, K.M., and Chklovskii, D.B. (2010). Ultrastructural analysis of hippocampal neuropil from the connectomics perspective. Neuron 67, 1009–1020.
Montero, V.M., Guillery, R.W., and Woolsey, C.N. (1977). Retinotopic organization within the thalamic reticular nucleus demonstrated by a double label autoradiographic technique. Brain Res. 138, 407–421.
Morosan, P., Rademacher, J., Schleicher, A., Amunts, K., Schormann, T., and Zilles, K. (2001). Human primary auditory cortex: cytoarchitectonic subdivisions and mapping into a spatial reference system. Neuroimage 13, 684–701.
Nelson, R.J. (2001). The Somatosensory System: Deciphering the Brain’s Own Body Image (CRC Press).
Nolte, J. (2002). The Human Brain: An Introduction to Its Functional Anatomy (Mosby).
Ohki, K., Chung, S., Chung, Y.H., Kara, P., and Reid, R.C. (2005). Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Neuron 433, 597–603.
Parrish, J.Z., Emoto, K., Kim, M.D., and Jan, Y.N. (2007). Mechanisms that regulate establishment, maintenance, and remodeling of dendritic fields. Annu. Rev. Neurosci. 30, 399–423.
Peters, A. (1979). Thalamic input to the cerebral cortex. Trends Neurosci. 2, 183.
Pickles, J.O. (2012). An Introduction to the Physiology of Hearing (Academic Press).
Raff, M.C., Whitmore, A. V., and Finn, J.T. (2002). Axonal Self-Destruction and Neurodegeneration. Science (80-. ). 296, 868–871.
Rivera-Alba, M., Vitaladevuni, S.N., Mishchenko, Y., Mischenko, Y., Lu, Z., Takemura, S.-Y., Scheffer, L., Meinertzhagen, I. a, Chklovskii, D.B., and de Polavieja, G.G. (2011). Wiring economy and volume exclusion determine neuronal placement in the Drosophila brain. Curr. Biol. 21, 2000–2005.
Sandler, S.I. (2010). An Introduction to Applied Statistical Thermodynamics (John Wiley & Sons).
Schaeffer, K. (1892). Beitrag zur Histologie der Ammonshornformation. Arch Mikrosc Anat 39, 611–632.
Scheff, S.W., Price, D.A., Schmitt, F.A., and Mufson, E.J. (2006). Hippocampal synaptic loss in early Alzheimer’s disease and mild cognitive impairment. Neurobiol. Aging 27, 1372–1384.
Shepherd, G.M., and Harris, K.M. (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.
Sorra, K.E., and Harris, K.M. (2000). Overview on the structure, composition, function, development, and plasticity of hippocampal dendritic spines. Hippocampus 10, 501–511.
Sporns, O., Chialvo, D.R., Kaiser, M., and Hilgetag, C.C. (2004). Organization, development and function of complex brain networks. Trends Cogn. Sci. 8, 418–426.
Sporns, O., Tononi, G., Kötter, R., Kotter, R., Kötter, R., and Kotter, R. (2005). The human connectome: a structural description of the human brain. PLoS Comput. Biol. 1, e42.
Stepanyants, A., and Chklovskii, D.B. (2005). Neurogeometry and potential synaptic connectivity. TRENDS Neurosci. 28, 387.
Stepanyants, A., Hirsch, J.A., Martinez, L.M., Kisvarday, Z.F., Ferecsko, A.S., and Chklovskii, D.B. (2008). Local Potential Connectivity in Cat Primary Visual Cortex. Cereb. Cortex 18, 13–28.
Tear, G. (1999). Neuronal guidance: a genetic perspective. Trends Neurosci. 15, 113–118.
Terry, R.D. (2000). Cell Death or Synaptic Loss in Alzheimer Disease. J. Neuropathol. Exp. Neurol. 59, 1118–1119.
Uhlhaas, P.J., and Singer, W. (2006). Neural Synchrony in Brain Disorders: Relevance for Cognitive Dysfunctions and Pathophysiology. Neuron 52, 155–168.
Varshney, L.R., Sjöström, P.J., and Chklovskii, D.B. (2006). Optimal information storage in noisy synapses under resource constraints. Neuron 52, 409–423.
Westrum, L.E., and Blackstad, T.W. (1962). An electron microscopic study of the stratum radiatum of the rat hippocampus (regio superior, CA1) with particular emphasis on synaptology. J. Comput. Neurol. 119, 281–309.
Wolf, L., Goldberg, C., Manor, N., Sharan, R., and Ruppin, E. (2011). Gene expression in the rodent brain is associated with its regional connectivity. PLoS Comput. Biol. 7, e1002040.
Wong, R.O.L. (1999). Retinal waves and visual system development. Annu. Rev. Neurosci. 22, 29–47.
Adams, D.L., and Horton, J.C. (2003). A Precise Retinotopic Map of Primate Striate Cortex Generated from the Representation of Angioscotomas. J. Neurosci. 23, 3771–3789.
Amaral, D.G., and Witter, M.P. (1989). The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31, 571–591.
Arbib, M.A., Erdi, P., and Szentagothai, J. (1997). Neural Organization: Structure, Function, and Dynamics (A Bradford Book).
Bonda, D.J., Bajić, V.P., Spremo-Potparevic, B., Casadesus, G., Zhu, X., Smith, M.A., and Lee, H.-G. (2010). Review: Cell cycle aberrations and neurodegeneration. Neuropathol. Appl. Neurobiol. 36, 157–163.
de Bono, M., Villu Maricq, A., Bono, M., Villu Maricq, A., de Bono, M., V., M.A., and Villu Maricq, A. (2005). Neuronal substrates of complex behaviors in C. elegans. Annu. Rev. Neurosci. 28, 451–501.
Bosking, W.H.W.W.H.W., Zhang, Y., Schofield, B., and Fitzpatrick, D. (1997). Orientation Selectivity and the Arrangement of Horizontal Connections in Tree Shrew Striate Cortex. J. Neurosci. 17, 2112.
Braitenberg, V., and Schuz, A. (1998). Cortex: statistics and geometry of neuronal connectivity. (Berlin: Springer).
Brambilla, P., Hardan, A., di Nemi, S.U., Perez, J., Soares, J.C., and Barale, F. (2003). Brain anatomy and development in autism: Review of structural MRI studies. Brain Res. Bull. 61, 557–569.
Brodmann, K., and Garey, L.J. (2005). Brodmann’s: Localisation in the Cerebral Cortex (Springer).
Cajal, R. (1909). Histologie du systeme nerveux de l’homme et des vertebres (Paris: Madrid, Instituto Ramon y Cajal).
Castellanos, F.X., Lee, P.P., Sharp, W., Jeffries, N.O., Greenstein, D.K., Clasen, L.S., Blumenthal, J.D., James, R.S., Ebens, C.L., Walter, J.M., et al. (2002). Developmental Trajectories of Brain Volume Abnormalities in Children and Adolescents With Attention-Deficit/Hyperactivity Disorder. J. Am. Med. Assoc. 288, 1740–1748.
Chandler, D. (1987). Introduction to Modern Statistical Mechanics (New York: Oxford University Press).
Chklovskii, D.B.D.B.D.B.D.B.D.B., Schikorski, T., and Stevens, C.F. (2002). Wiring optimization in cortical circuits. Neuron 34, 341–347.
Damasio, H. (2005). Human Brain Anatomy in Computerized Images (Oxford university press).
Dickson, B.J. (2002). Molecular mechanisms of axon guidance. Science (80-. ). 298, 1959–1964.
Erwin, E., Obermayer, K., and Schulten, K. (1995). Models of Orientation and Ocular Dominance Columns in the Visual Cortex: A Critical Comparison. Neural Comput. 7, 425–468.
Ferster, D., and Miller, K.D. (2000). Neural Mechanisms of Orientation Selectivity in the Visual Cortex. Annu. Rev. Neurosci. 23, 441–471.
Fiala, J.C., Kirov, S.A., Feinberq, M.D., Petrak, L.J., George, P., Goddard, C.A., and Harris, K.M. (2003). Timing of neuronal and glial ultrastructure disruption during brain slice preparation and recovery in vitro. J. Comput. Neurol. 465, 90–103.
Freeman, R.D.D. (2003). Cortical columns: a multi-parameter examination. Cereb. Cortex 13, 70.
Garrard, P., Patterson, K., Watson, P.C., and Hodges, J.R. (1998). Category specific semantic loss in dementia of Alzheimer’s type. Functional-anatomical correlations from cross-sectional analyses. Brain 121, 633–646.
Geschwind, N. (1975). The Apraxias: Neural Mechanisms of Disorders of Learned Movement. Am. Sci. 63, 188–195.
Good, C.D., Scahill, R.I., Fox, N.C., Ashburner, J., Friston, K.J., Chan, D., Crum, W.R., Rossor, M.N., and Frackowiak, R.S.J. (2002). Automatic Differentiation of Anatomical Patterns in the Human Brain: Validation with Studies of Degenerative Dementias. Neuroimage 17, 29–46.
Hamos, J.E., DeGennaro, L.J., and Drachman, D.A. (1989). Synaptic loss in Alzheimer’s disease and other dementias. Neurology 39, 355.
Harris, K.M., and Stevens, J.K. (1989). Dendritic spines of CA1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J. Neurosci. 9, 2982–2997.
Hatton, G.I. (1990). Emerging concepts of structure-function dynamics in adult brain: the hypothalamo-neurohypophysial system. Prog. Neurobiol. 34, 437–504.
Jaynes, E.T. (2003). Probability Theory: The Logic of Science. (New York: Cambridge University Press).
Kandel, E., Schwartz, J., and Jessell, T. (2000). Principles of Neural Science (McGraw-Hill Medical).
Keil, W., Schmidt, K.F., Löwel, S., and Kaschube, M. (2010). Reorganization of columnar architecture in the growing visual cortex. Proc. Natl. Acad. Sci. 107, 12293.
McLaughlin, T., and O’Leary, D.M. (2005). Molecular gradients and development of retinotopic maps. Annu. Rev. Neurosci. 28, 327–355.
McQuarrie, D.A. (2000). Statistical Mechanics (University Science Books).
Miller, K.D., Keller, J.B., and Stryker, M.P. (1989). Ocular dominance column development: analysis and simulation. Science (80-. ). 245, 605–615.
Mishchenko, Y. (2009). Automation of 3D reconstruction of neural tissue from large volume of conventional serial section transmission electron micrographs. J. Neurosci. Methods 176, 276–289.
Mishchenko, Y. (2015). A function for fast computation of large discrete Euclidean distance transforms in three or more dimensions in Matlab. Signal, Image Video Process. 9, 19.
Mishchenko, Y., and Paninski, L. (2012). Efficient methods for sampling spike trains in networks of coupled neurons. Ann. Appl. Stat. 5, 1893–1919.
Mishchenko, Y., Hu, T., Spacek, J., Mendenhall, J., Harris, K.M., and Chklovskii, D.B. (2010). Ultrastructural analysis of hippocampal neuropil from the connectomics perspective. Neuron 67, 1009–1020.
Montero, V.M., Guillery, R.W., and Woolsey, C.N. (1977). Retinotopic organization within the thalamic reticular nucleus demonstrated by a double label autoradiographic technique. Brain Res. 138, 407–421.
Morosan, P., Rademacher, J., Schleicher, A., Amunts, K., Schormann, T., and Zilles, K. (2001). Human primary auditory cortex: cytoarchitectonic subdivisions and mapping into a spatial reference system. Neuroimage 13, 684–701.
Nelson, R.J. (2001). The Somatosensory System: Deciphering the Brain’s Own Body Image (CRC Press).
Nolte, J. (2002). The Human Brain: An Introduction to Its Functional Anatomy (Mosby).
Ohki, K., Chung, S., Chung, Y.H., Kara, P., and Reid, R.C. (2005). Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Neuron 433, 597–603.
Parrish, J.Z., Emoto, K., Kim, M.D., and Jan, Y.N. (2007). Mechanisms that regulate establishment, maintenance, and remodeling of dendritic fields. Annu. Rev. Neurosci. 30, 399–423.
Peters, A. (1979). Thalamic input to the cerebral cortex. Trends Neurosci. 2, 183.
Pickles, J.O. (2012). An Introduction to the Physiology of Hearing (Academic Press).
Raff, M.C., Whitmore, A. V., and Finn, J.T. (2002). Axonal Self-Destruction and Neurodegeneration. Science (80-. ). 296, 868–871.
Rivera-Alba, M., Vitaladevuni, S.N., Mishchenko, Y., Mischenko, Y., Lu, Z., Takemura, S.-Y., Scheffer, L., Meinertzhagen, I. a, Chklovskii, D.B., and de Polavieja, G.G. (2011). Wiring economy and volume exclusion determine neuronal placement in the Drosophila brain. Curr. Biol. 21, 2000–2005.
Sandler, S.I. (2010). An Introduction to Applied Statistical Thermodynamics (John Wiley & Sons).
Schaeffer, K. (1892). Beitrag zur Histologie der Ammonshornformation. Arch Mikrosc Anat 39, 611–632.
Scheff, S.W., Price, D.A., Schmitt, F.A., and Mufson, E.J. (2006). Hippocampal synaptic loss in early Alzheimer’s disease and mild cognitive impairment. Neurobiol. Aging 27, 1372–1384.
Shepherd, G.M., and Harris, K.M. (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.
Sorra, K.E., and Harris, K.M. (2000). Overview on the structure, composition, function, development, and plasticity of hippocampal dendritic spines. Hippocampus 10, 501–511.
Sporns, O., Chialvo, D.R., Kaiser, M., and Hilgetag, C.C. (2004). Organization, development and function of complex brain networks. Trends Cogn. Sci. 8, 418–426.
Sporns, O., Tononi, G., Kötter, R., Kotter, R., Kötter, R., and Kotter, R. (2005). The human connectome: a structural description of the human brain. PLoS Comput. Biol. 1, e42.
Stepanyants, A., and Chklovskii, D.B. (2005). Neurogeometry and potential synaptic connectivity. TRENDS Neurosci. 28, 387.
Stepanyants, A., Hirsch, J.A., Martinez, L.M., Kisvarday, Z.F., Ferecsko, A.S., and Chklovskii, D.B. (2008). Local Potential Connectivity in Cat Primary Visual Cortex. Cereb. Cortex 18, 13–28.
Tear, G. (1999). Neuronal guidance: a genetic perspective. Trends Neurosci. 15, 113–118.
Terry, R.D. (2000). Cell Death or Synaptic Loss in Alzheimer Disease. J. Neuropathol. Exp. Neurol. 59, 1118–1119.
Uhlhaas, P.J., and Singer, W. (2006). Neural Synchrony in Brain Disorders: Relevance for Cognitive Dysfunctions and Pathophysiology. Neuron 52, 155–168.
Varshney, L.R., Sjöström, P.J., and Chklovskii, D.B. (2006). Optimal information storage in noisy synapses under resource constraints. Neuron 52, 409–423.
Westrum, L.E., and Blackstad, T.W. (1962). An electron microscopic study of the stratum radiatum of the rat hippocampus (regio superior, CA1) with particular emphasis on synaptology. J. Comput. Neurol. 119, 281–309.
Wolf, L., Goldberg, C., Manor, N., Sharan, R., and Ruppin, E. (2011). Gene expression in the rodent brain is associated with its regional connectivity. PLoS Comput. Biol. 7, e1002040.
Wong, R.O.L. (1999). Retinal waves and visual system development. Annu. Rev. Neurosci. 22, 29–47.