Abstract
The axonal projections of nerve cells have been used to infer synaptic connectivity ever since the drawings of Ramon y Cajal more than a hundred years ago. Here we review the assumptions behind these studies and report how axonal projections of thalamic and cortical neurons can be used to anatomically define cortical columns as innervation volumes in rat barrel cortex. We then apply this analysis to cortical interneurons and illustrate that it is the axonal projections of interneurons which best permit their functional classification with reference to cortical columns. We conclude that the axons of cortical nerve cells should serve as their primary classifiers, because they best indicate their function in the neocortical neuronal network.
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References
Ascoli GA et al (2008) Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 9:557–568
Bacci A, Huguenard JR, Prince DA (2004) Long-lasting self-inhibition of neocortical interneurons mediated by endocannabinoids. Nature 431:312–316
Bender KJ, Rangel J, Feldman DE (2003) Development of columnar topography in the excitatory layer 4 to layer 2/3 projection in rat barrel cortex. J Neurosci 23:8759–8770
Bloom FE, Ueda T, Battenberg E, Greengard P (1979) Immunocytochemical localization, in synapses, of protein I, an endogenous substrate for protein kinases in mammalian brain. Proc Natl Acad Sci USA 76:5982–5986
Braitenberg V, Schüz A (1998) Cortex: Statistics and Geometry of Neuronal Connectivity. Springer, Berlin Heidelberg
Chen BL, Hall DH, Chklovskii DB (2006) Wiring optimization can relate neuronal structure and function. Proc Natl Acad Sci USA 103:4723–4728
Chmielowska J, Carvell GE, Simons DJ (1989) Spatial organization of thalamocortical and corticothalamic projection systems in the rat SmI barrel cortex. J Comp Neurol 285:325–338
Colonnier M (1964) Experimental degeneration in the cerebral cortex. J Anat 98:47–53
Colonnier M (1968) Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. Brain Res 9:268–287
Cowan WM, Gottlieb DI, Hendrickson AE, Price JL, Woolsey TA (1972) The autoradiographic demonstration of axonal connections in the central nervous system. Brain Res 37:21–51
Dantzker JL, Callaway EM (2000) Laminar sources of synaptic input to cortical inhibitory interneurons and pyramidal neurons. Nat Neurosci 3:701–707
De Camilli P, Cameron R, Greengard P (1983) Synapsin I (protein I), a nerve terminal-specific phosphoprotein. I. Its general distribution in synapses of the central and peripheral nervous system demonstrated by immunofluorescence in frozen and plastic sections. J Cell Biol 96:1337–1354
Denk W, Horstmann H (2004) Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLoS Biol 2:e329
Evans DH, Hamlyn LH (1956) A study of silver degeneration methods in the central nervous system. J Anat 90:193–203
Feldmeyer D, Egger V, Lübke J, Sakmann B (1999) Reliable synaptic connections between pairs of excitatory layer 4 neurones within a single ‘barrel’ of developing rat somatosensory cortex. J Physiol 521:169–190
Feldmeyer D, Lübke J, Silver RA, Sakmann B (2002) Synaptic connections between layer 4 spiny neurone-layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column. J Physiol 538:803–822
Gilbert CD, Wiesel TN (1979) Morphology and intracortical projections of functionally characterised neurones in the cat visual cortex. Nature 280:120–125
Glees P (1946) Terminal degeneration within the central nervous system as studied by a new silver method. J Neuropath Exp Neurol 5:54–59
Gray EG (1959) Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study. J Anat 93:420–433
Gray EG, Hamlyn LH (1962) Electron microscopy of experimental degeneration in the avian optic tectum. J Anat 96: 305, 309–316
Grutzendler J, Kasthuri N, Gan WB (2002) Long-term dendritic spine stability in the adult cortex. Nature 420:812–816
Gupta A, Wang Y, Markram H (2000) Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287:273–278
Helmstaedter M, Briggman KL, Denk W (2008a) 3D structural imaging of the brain with photons and electrons. Curr Opin Neurobiol 18:633–641
Helmstaedter M, Staiger JF, Sakmann B, Feldmeyer D (2008b) Efficient recruitment of layer 2/3 interneurons by layer 4 input in single columns of rat somatosensory cortex. J Neurosci 28:8273–8284
Helmstaedter M, Sakmann B, Feldmeyer D (2009a) L2/3 interneuron groups defined by multiparameter analysis of axonal projection, dendritic geometry, and electrical excitability. Cereb Cortex 19:951–962
Helmstaedter M, Sakmann B, Feldmeyer D (2009b) Neuronal correlates of local, lateral, and translaminar inhibition with reference to cortical columns. Cereb Cortex 19:926–937
Helmstaedter M, Sakmann B, Feldmeyer D (2009c) The relation between dendritic geometry, electrical excitability, and axonal projections of L2/3 interneurons in rat barrel cortex. Cereb Cortex 19:938–950
Herkenham M (1980) Laminar organization of thalamic projections to the rat neocortex. Science 207:532–535
Hoff EC (1932) Central nerve T’erminals in the mammalian spinal cord and their examination by experimental degeneration. Proc R Soc Lond B Biol Sci 111:175–188
Hubel DH, Wiesel TN (1968) Receptive fields and functional architecture of monkey striate cortex. J Physiol 195:215–243
Hubel DH, Wiesel TN (1969) Anatomical demonstration of columns in the monkey striate cortex. Nature 221:747–750
Jones EG (2007) Neuroanatomy: Cajal and after Cajal. Brain Res Rev 55:248–255
Jones EG, Powell TP (1970) An electron microscopic study of the laminar pattern and mode of termination of afferent fibre pathways in the somatic sensory cortex of the cat. Philos Trans R Soc Lond B Biol Sci 257:45–62
Killackey HP (1973) Anatomical evidence for cortical subdivisions based on vertically discrete thalamic projections from the ventral posterior nucleus to cortical barrels in the rat. Brain Res 51:326–331
Lasek R, Joseph BS, Whitlock DG (1968) Evaluation of a radioautographic neuroanatomical tracing method. Brain Res 8:319–336
LeVay S, Gilbert CD (1976) Laminar patterns of geniculocortical projection in the cat. Brain Res 113:1–19
Lichtman JW, Smith SJ (2008) Seeing circuits assemble. Neuron 60:441–448
Lorente de No R (1922) La corteza cerebral de ratón Trabajos del Laboratorio de Investigaciones Biológicas de la Universidad de Madrid 20:41–78
Lorente de No R (1938) Cerebral cortex: architecture, intracortical connections, motor projections (ch. 15). In: Fulton JF (ed) Physiology of the nervous system. Oxford University Press, Oxford, pp 288–313
Lorente de No R (1992) The cerebral cortex of the mouse (A first contribution – the “acoustic” cortex). (Trans: Fairén A, Regidor J, Kruger L). Somat Mot Res 9:3–36
Lu SM, Lin RC (1993) Thalamic afferents of the rat barrel cortex: a light- and electron-microscopic study using Phaseolus vulgaris leucoagglutinin as an anterograde tracer. Somatosens Mot Res 10:1–16
Lübke J, Egger V, Sakmann B, Feldmeyer D (2000) Columnar organization of dendrites and axons of single and synaptically coupled excitatory spiny neurons in layer 4 of the rat barrel cortex. J Neurosci 20:5300–5311
Lübke J, Roth A, Feldmeyer D, Sakmann B (2003) Morphometric analysis of the columnar innervation domain of neurons connecting layer 4 and layer 2/3 of juvenile rat barrel cortex. Cereb Cortex 13:1051–1063
Magrassi L, Purves D, Lichtman JW (1987) Fluorescent probes that stain living nerve terminals. J Neurosci 7:1207–1214
Mainen ZF, Sejnowski TJ (1996) Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382:363–366
Markram H, Lübke J, Frotscher M, Roth A, Sakmann B (1997) Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J Physiol 500:409–440
Micheva KD, Smith SJ (2007) Array tomography: a new tool for imaging the molecular architecture and ultrastructure of neural circuits. Neuron 55:25–36
Mountcastle VB (1957) Modality and topographic properties of single neurons of cat’s somatic sensory cortex. J Neurophysiol 20:408–434
Mountcastle VB (1997) The columnar organization of the neocortex. Brain 120 (Pt 4):701–722
Peters A (1979) Thalamic input to the cerebral cortex. Trends Neurosci 2:183–185
Peters A (2007) Golgi, Cajal, and the fine structure of the nervous system. Brain Res Rev 55:256–263
Ramón y Cajal S (1904) Textura del sistema nervioso del hombre y de los vertebrados. Imprenta N. Moya, Madrid
Ramón y Cajal S (1995) Histology of the nervous system. Oxford University Press, New York, Oxford
Schaefer AT, Larkum ME, Sakmann B, Roth A (2003) Coincidence detection in pyramidal neurons is tuned by their dendritic branching pattern. J Neurophysiol 89:3143–3154
Shepherd GM, Stepanyants A, Bureau I, Chklovskii D, Svoboda K (2005) Geometric and functional organization of cortical circuits. Nat Neurosci 8:782–790
Sholl DA (1953) Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 87:387–406
Sholl DA (1955) The organization of the visual cortex in the cat. J Anat 89:33–46
Silver RA, Lübke J, Sakmann B, Feldmeyer D (2003) High-probability uniquantal transmission at excitatory synapses in barrel cortex. Science 302:1981–1984
Stepanyants A, Chklovskii DB (2005) Neurogeometry and potential synaptic connectivity. Trends Neurosci 28:387–394
Stepanyants A, Hirsch JA, Martinez LM, Kisvarday ZF, Ferecsko AS, Chklovskii DB (2008) Local potential connectivity in cat primary visual cortex. Cereb Cortex 18:13–28
Taylor AC, Weiss P (1965) Demonstration of axonal flow by the movement of tritium-labeled protein in mature optic nerve fibers. Proc Natl Acad Sci USA 54:1521–1527
Trachtenberg JT, Chen BE, Knott GW, Feng G, Sanes JR, Welker E, Svoboda K (2002) Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420:788–794
Uchizono K (1965) Characteristics of excitatory and inhibitory synapses in the central nervous system of the cat. Nature 207:642–643
Walker AE (1936) An experimental study of the thalamocortical projection of the macaque monkey. J Comp Neurol 64:1–39
White EL (1979) Thalamocortical synaptic relations: a review with emphasis on the projections of specific thalamic nuclei to the primary sensory areas of the neocortex. Brain Res 180:275–311
White EL (2007) Reflections on the specificity of synaptic connections. Brain Res Rev 55:422–429
White EL, Keller A (1989) Cortical circuits: synaptic organization of the cerebral cortex: structure, function, and theory. Birkhäuser, Boston
White JG, Southgate E, Thomson JN, Brenner S (1986) The structure of the nervous system of the nematode caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 314:1–340
Wise SP, Jones EG (1978) Developmental studies of thalamocortical and commissural connections in the rat somatic sensory cortex. J Comp Neurol 178:187–208
Woolsey TA, Van der Loos H (1970) The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res 17:205–242.
Acknowledgments
We are grateful to Bert Sakmann for inspiration, guidance, and continued support of many of the studies summarized in this chapter, and to the Max Planck Society and the Helmholtz Alliance for Systems Biology for funding.
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Helmstaedter, M., Feldmeyer, D. (2010). Axons Predict Neuronal Connectivity Within and Between Cortical Columns and Serve as Primary Classifiers of Interneurons in a Cortical Column. In: Feldmeyer, D., Lübke, J. (eds) New Aspects of Axonal Structure and Function. Springer, Boston, MA. https://doi.org/10.1007/978-1-4419-1676-1_8
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