Development of layer‐specific axonal arborizations in mouse primary somatosensory cortex

In the developing neocortex, pyramidal neurons use molecular cues to form axonal arbors selectively in the correct layers. Despite the utility of mice for molecular and genetic studies, little work has been done on the development of layer‐specific axonal arborizations of pyramidal neurons in mice. We intracellularly labeled and reconstructed the axons of layer 2/3 and layer 5 pyramidal neurons in slices of primary somatosensory cortex from C57Bl6 mice on postnatal days 7–21. For all neurons studied, the development of the axonal arborizations in mice follows a pattern similar to that seen in other species; laminar specificity of the earliest axonal branches is similar to that of mature animals. At P7, pyramidal neurons are very simple, having only a main descending axon and few primary branches. Between P7 and P10, there is a large increase in the total number of axonal branches, and axons continue to increase in complexity and total length from P10 to P21. Unlike observations in ferrets, cats, and monkeys, two types of layer 2/3 pyramidal neurons are present in both mature and developing mice; cells in superficial layer 2/3 lack axonal arbors in layer 4, and cells close to the layer 4 border have substantial axonal arbors within layer 4. We also describe axonal and dendritic arborization patterns of three pyramidal cell types in layer 5. The axons of tall‐tufted layer 5 pyramidal neurons arborize almost exclusively within deep layers while tall‐simple, and short layer 5 pyramidal neurons also project axons to superficial layers. J. Comp. Neurol. 494:398–414, 2006. © 2005 Wiley‐Liss, Inc.

[1]  B. Gähwiler,et al.  Selective neurofilament (SMI-32, FNP-7 and N200) expression in subpopulations of layer V pyramidal neurons in vivo and in vitro. , 2004, Cerebral cortex.

[2]  N Yamamoto,et al.  Neural connections between the lateral geniculate nucleus and visual cortex in vitro. , 1989, Science.

[3]  D. O'Leary,et al.  Target control of collateral extension and directional axon growth in the mammalian brain. , 1990, Science.

[4]  L C Katz,et al.  Local circuitry of identified projection neurons in cat visual cortex brain slices , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  Edward M Callaway,et al.  Reorganization of Exuberant Axonal Arbors Contributes to the Development of Laminar Specificity in Ferret Visual Cortex , 2002, The Journal of Neuroscience.

[6]  E. Callaway,et al.  Cytochrome-oxidase blobs and intrinsic horizontal connections of layer 2/3 pyramidal neurons in primate V1 , 1998, Visual Neuroscience.

[7]  D. O'Leary,et al.  Functional classes of cortical projection neurons develop dendritic distinctions by class-specific sculpting of an early common pattern , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  B. Connors,et al.  Apical dendrites of the neocortex: correlation between sodium- and calcium-dependent spiking and pyramidal cell morphology , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  Walther Akemann,et al.  Transgenic mice expressing a fluorescent in vivo label in a distinct subpopulation of neocortical layer 5 pyramidal cells , 2004, The Journal of comparative neurology.

[10]  M. Miller,et al.  Maturation of rat visual cortex. III. Postnatal morphogenesis and synaptogenesis of local circuit neurons. , 1986, Brain research.

[11]  S. Wise,et al.  Somatotopic and columnar organization in the corticotectal projection of the rat somatic sensory cortex , 1977, Brain Research.

[12]  P. Rakić Neurons in Rhesus Monkey Visual Cortex: Systematic Relation between Time of Origin and Eventual Disposition , 1974, Science.

[13]  E. Callaway,et al.  Development of axonal arbors of layer 6 pyramidal neurons in ferret primary visual cortex , 1996, The Journal of comparative neurology.

[14]  R. Sidman,et al.  Autoradiographic Study of Cell Migration during Histogenesis of Cerebral Cortex in the Mouse , 1961, Nature.

[15]  Rafael Yuste,et al.  Quantitative morphologic classification of layer 5 neurons from mouse primary visual cortex , 2003, The Journal of comparative neurology.

[16]  J. Bolz,et al.  Formation of specific afferent connections in organotypic slice cultures from rat visual cortex cocultured with lateral geniculate nucleus , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  D. Prince,et al.  Burst generating and regular spiking layer 5 pyramidal neurons of rat neocortex have different morphological features , 1990, The Journal of comparative neurology.

[18]  Tobias Bonhoeffer,et al.  Formation of target-specific neuronal projections in organotypic slice cultures from rat visual cortex , 1990, Nature.

[19]  J. Winer,et al.  Layer V in rat auditory cortex: Projections to the inferior colliculus and contralateral cortex , 1988, Hearing Research.

[20]  J. Lund,et al.  Development of neurons in the visual cortex (area 17) of the monkey (Macaca nemestrina): A Golgi study from fetal day 127 to postnatal maturity , 1977, The Journal of comparative neurology.

[21]  A. Peters,et al.  Maturation of rat visual cortex. II. A combined Golgi‐electron microscope study of pyramidal neurons , 1981, The Journal of comparative neurology.

[22]  C. Blakemore,et al.  Pyramidal neurons in layer 5 of the rat visual cortex. III. Differential maturation of axon targeting, dendritic morphology, and electrophysiological properties , 1994, The Journal of comparative neurology.

[23]  E. Callaway Local circuits in primary visual cortex of the macaque monkey. , 1998, Annual review of neuroscience.

[24]  D. O'Leary,et al.  Selective elimination of axons extended by developing cortical neurons is dependent on regional locale: experiments utilizing fetal cortical transplants , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  C. Gilbert Microcircuitry of the visual cortex. , 1983, Annual review of neuroscience.

[26]  C Blakemore,et al.  Morphology and Growth Patterns of Developing Thalamocortical Axons , 2000, The Journal of Neuroscience.

[27]  V. Castellani,et al.  Dual Action of a Ligand for Eph Receptor Tyrosine Kinases on Specific Populations of Axons during the Development of Cortical Circuits , 1998, The Journal of Neuroscience.

[28]  Michael Miller Maturation of rat visual cortex. I. A quantitative study of Golgi-impregnated pyramidal neurons , 1981, Journal of neurocytology.

[29]  N Yamamoto,et al.  Stop and Branch Behaviors of Geniculocortical Axons: A Time-Lapse Study in Organotypic Cocultures , 1997, The Journal of Neuroscience.

[30]  J. S. McCasland,et al.  Cortical local circuit axons do not mature after early deafferentation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[31]  D. McCormick,et al.  Control of firing mode of corticotectal and corticopontine layer V burst-generating neurons by norepinephrine, acetylcholine, and 1S,3R- ACPD , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  D. O'Leary,et al.  Connectional distinction between callosal and subcortically projecting cortical neurons is determined prior to axon extension. , 1993, Developmental biology.

[33]  Zhong-Wei Zhang,et al.  Maturation of layer V pyramidal neurons in the rat prefrontal cortex: intrinsic properties and synaptic function. , 2004, Journal of neurophysiology.

[34]  Kristina D. Micheva,et al.  Quantitative aspects of synaptogenesis in the rat barrel field cortex with special reference to GABA circuitry , 1996, The Journal of comparative neurology.

[35]  K. Martin Neuronal Circuits in Cat Striate Cortex , 1984 .

[36]  D. O'Leary,et al.  Cortical axons branch to multiple subcortical targets by interstitial axon budding: Implications for target recognition and “waiting periods” , 1988, Neuron.

[37]  C. Shatz,et al.  Neurogenesis of the cat's primary visual cortex , 1985, The Journal of comparative neurology.

[38]  Jürgen Bolz,et al.  How do wiring molecules specify cortical connections? , 1997, Cell and Tissue Research.

[39]  E M Callaway,et al.  Prenatal Development of Layer-Specific Local Circuits in Primary Visual Cortex of the Macaque Monkey , 1998, The Journal of Neuroscience.

[40]  A. Larkman,et al.  Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. II. Electrophysiology , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  M. Hübener,et al.  Guidance of Thalamocortical Axons by Growth‐promoting Molecules in Developing Rat Cerebral Cortex , 1995, The European journal of neuroscience.

[42]  J. Bolz,et al.  Morphological types of projection neurons in layer 5 of cat visual cortex , 1990, The Journal of comparative neurology.

[43]  B. Schofield,et al.  Dendritic morphology and axon collaterals of corticotectal, corticopontine, and callosal neurons in layer V of primary visual cortex of the hooded rat , 1988, The Journal of comparative neurology.

[44]  A. Larkman,et al.  Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. I. Establishment of cell classes , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  D. O'Dowd,et al.  Aspects of early postnatal development of cortical neurons that proceed independently of normally present extrinsic influences. , 1993, Journal of neurobiology.

[46]  V. Caviness,et al.  Sequence of Neuron Origin and Neocortical Laminar Fate: Relation to Cell Cycle of Origin in the Developing Murine Cerebral Wall , 1999, The Journal of Neuroscience.

[47]  J. Bolz,et al.  Membrane-bound molecules in rat cerebral cortex regulate thalamic innervation , 1992 .

[48]  J. Lund,et al.  Anatomical organization of macaque monkey striate visual cortex. , 1988, Annual review of neuroscience.

[49]  J. Bolz,et al.  Membrane-associated molecules regulate the formation of layer-specific cortical circuits. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[50]  Daniel E Feldman,et al.  Development of Columnar Topography in the Excitatory Layer 4 to Layer 2/3 Projection in Rat Barrel Cortex , 2003, The Journal of Neuroscience.

[51]  D. Price,et al.  The fates of cells generated at the end of neurogenesis in developing mouse cortex. , 2001, Journal of neurobiology.

[52]  E. Callaway,et al.  Laminar Specificity of Local Circuits in Barrel Cortex of Ephrin-A5 Knockout Mice , 2000, Journal of Neuroscience.

[53]  E. Callaway,et al.  Development of axonal arbors of layer 4 spiny neurons in cat striate cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  A. Burkhalter,et al.  Development of local circuits in human visual cortex , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  K. Toyama,et al.  Laminar specificity of extrinsic cortical connections studied in coculture preparations , 1992, Neuron.

[56]  V. Caviness Neocortical histogenesis in normal and reeler mice: a developmental study based upon [3H]thymidine autoradiography. , 1982, Brain research.

[57]  H. Killackey,et al.  Development and plasticity of local intracortical projections within the vibrissae representation of the rat primary somatosensory cortex , 1996, The Journal of comparative neurology.

[58]  M. Ishida,et al.  Distinct neuronal populations specified to form corticocortical and corticothalamic projections from layer VI of developing cerebral cortex , 2002, Neuroscience.

[59]  J. Bolz,et al.  Specification of layer-specific connections in the developing cortex. , 1996, Progress in brain research.

[60]  C. Shatz,et al.  Synaptic Activity and the Construction of Cortical Circuits , 1996, Science.

[61]  H. Kennedy,et al.  The timetable of laminar neurogenesis contributes to the specification of cortical areas in mouse isocortex , 1997, The Journal of comparative neurology.

[62]  K. Fox,et al.  Glutamate receptor blockade alters the development of intracortical connections in rat barrel cortex , 2003, Somatosensory & motor research.

[63]  A. Burkhalter,et al.  Intrinsic connections of rat primary visual cortex: Laminar organization of axonal projections , 1989, The Journal of comparative neurology.

[64]  E. Callaway,et al.  The Development of Local, Layer-Specific Visual Cortical Axons in the Absence of Extrinsic Influences and Intrinsic Activity , 1998, The Journal of Neuroscience.

[65]  E G Jones,et al.  Inhibitory synaptogenesis in mouse somatosensory cortex. , 1997, Cerebral cortex.

[66]  L C Katz,et al.  Development of local circuits in mammalian visual cortex. , 1992, Annual review of neuroscience.

[67]  T A Woolsey,et al.  Local intra‐ and interlaminar connections in mouse barrel cortex , 1990, The Journal of comparative neurology.

[68]  J. Bolz,et al.  Reconstructing cortical connections in a dish , 1993, Trends in Neurosciences.

[69]  J. Bolz,et al.  Morphology of identified projection neurons in layer 5 of rat visual cortex , 1988, Neuroscience Letters.

[70]  N. Novak,et al.  Formation of Specific Efferent Connections in Organotypic Slice Cultures from Rat Visual Cortex Cocultured with Lateral Geniculate Nucleus and Superior Colliculus , 1993, The European journal of neuroscience.

[71]  T. Woolsey,et al.  Postnatal growth of intrinsic connections in mouse barrel cortex , 2001, The Journal of comparative neurology.

[72]  L. C. Katz Specificity in the Development of Vertical Connections in Cat Striate Cortex , 1991, The European journal of neuroscience.

[73]  E M Callaway,et al.  Development of visual cortical axons: Layer‐specific effects of extrinsic influences and activity blockade , 2001, The Journal of comparative neurology.

[74]  T. L. Hickey,et al.  Visual cortex development in the ferret. I. Genesis and migration of visual cortical neurons , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[75]  H. Killackey,et al.  Laminar and areal differences in the origin of the subcortical projection neurons of the rat somatosensory cortex , 1989, The Journal of comparative neurology.

[76]  J. Olavarria,et al.  Beyond Laminar Fate: Toward a Molecular Classification of Cortical Projection/Pyramidal Neurons , 2003, Developmental Neuroscience.