Selective neurofilament (SMI-32, FNP-7 and N200) expression in subpopulations of layer V pyramidal neurons in vivo and in vitro.

There are two main types of layer V pyramidal neurons in rat cortex. Type I neurons have tufted apical dendrites extending into layer I, produce bursts of action potentials and project to subcortical targets (spinal cord, superior colliculus and pontine nuclei). Type II neurons have apical dendrites, which arborize in layers II-IV, do not produce bursts of action potentials and project to ipsilateral and contralateral cortex. The specific expression of different genes and proteins in these two distinct layer V neurons is unknown. To distinguish between distinct subpopulations, fluorescent microspheres were injected into subcortical targets (labeling type I neurons) or primary somatosensory cortex (labeling type II neurons) of adult rats. After transport, cortical sections were processed for immunohistochemistry using various antibodies. This study demonstrated that antigens recognized by SMI-32, N200 and FNP-7 antibodies were only expressed in subcortical (type I)--but not in contralateral (type II)--projecting neurons. NR1, NR2a/b, PLCbeta1, BDNF, NGF and TrkB antigens were highly expressed in all neuronal subpopulations examined. Organotypic culture experiments demonstrated that the development of neurofilament expression and laminar specificity does not depend on the presence of the subcortical targets. This study suggests specific markers for the subcortical projecting layer V neuron subpopulations.

[1]  J. Morrison,et al.  Progressive degeneration of nonphosphorylated neurofilament protein‐enriched pyramidal neurons predicts cognitive impairment in Alzheimer's disease: Stereologic analysis of prefrontal cortex area 9 , 2003, The Journal of comparative neurology.

[2]  J. Morrison,et al.  Stereologic analysis of neurofibrillary tangle formation in prefrontal cortex area 9 in aging and Alzheimer’s disease , 2003, Neuroscience.

[3]  J. Vickers,et al.  Neurofilament triplet proteins are restricted to a subset of neurons in the rat neocortex , 2002, Journal of Chemical Neuroanatomy.

[4]  Michael W. Miller Expression of nerve growth factor and its receptors in the somatosensory-motor cortex of Macaca nemestrina , 2000, Journal of neurocytology.

[5]  H Scheich,et al.  Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus). III. Anatomical subdivisions and corticocortical connections , 2000, The European journal of neuroscience.

[6]  K Zilles,et al.  Neurofilament protein distribution in the macaque monkey dorsolateral premotor cortex , 2000, The European journal of neuroscience.

[7]  C. Geula,et al.  Motor neurons are rich in non-phosphorylated neurofilaments: cross-species comparison and alterations in ALS , 2000, Brain Research.

[8]  A. Chaudhuri,et al.  Developmental profiles of SMI-32 immunoreactivity in monkey striate cortex. , 2000, Brain research. Developmental brain research.

[9]  S. Mcconnell,et al.  Cortical Neurons Require Otx1 for the Refinement of Exuberant Axonal Projections to Subcortical Targets , 1999, Neuron.

[10]  J. Hornung,et al.  Medium‐sized neurofilament protein related to maturation of a subset of cortical neurons , 1999, The Journal of comparative neurology.

[11]  J. Hornung,et al.  Dopamine Affects Parvalbumin Expression during Cortical Development In Vitro , 1999, The Journal of Neuroscience.

[12]  M. Hepp-Reymond,et al.  Parcellation of the lateral premotor cortex of the macaque monkey based on staining with the neurofilament antibody SMI-32 , 1999, Experimental Brain Research.

[13]  P. Barbaresi,et al.  Neuronal, glial, and epithelial localization of γ‐aminobutyric acid transporter 2, a high‐affinity γ‐aminobutyric acid plasma membrane transporter, in the cerebral cortex and neighboring structures , 1999, The Journal of comparative neurology.

[14]  E. Tongiorgi,et al.  Co-expression of TrkB and the N-methyl-d-aspartate receptor subunits NR1-C1, NR2A and NR2B in the rat visual cortex , 1999, Neuroscience.

[15]  Colin Blakemore,et al.  Development of Signals Influencing the Growth and Termination of Thalamocortical Axons in Organotypic Culture , 1999, Experimental Neurology.

[16]  Y. Agid,et al.  An immunohistochemical study of the distribution of brain-derived neurotrophic factor in the adult human brain, with particular reference to Alzheimer's disease , 1999, Neuroscience.

[17]  D. Graham,et al.  The neuronal cytoskeleton is at risk after mild and moderate brain injury. , 1998, Journal of neurotrauma.

[18]  R. Nixon Dynamic behavior and organization of cytoskeletal proteins in neurons: reconciling old and new findings , 1998, BioEssays : news and reviews in molecular, cellular and developmental biology.

[19]  M. Bickford,et al.  Neurofilament Proteins in Y-Cells of the Cat Lateral Geniculate Nucleus: Normal Expression and Alteration with Visual Deprivation , 1998, The Journal of Neuroscience.

[20]  J. Bohl,et al.  Monoclonal antibodies SMI 311 and SMI 312 as tools to investigate the maturation of nerve cells and axonal patterns in human fetal brain , 1998, Cell and Tissue Research.

[21]  Iwona Stepniewska,et al.  Multiple divisions of macaque precentral motor cortex identified with neurofilament antibody SMI-32 , 1997, Brain Research.

[22]  Leslie G. Ungerleider,et al.  Neurofilament protein is differentially distributed in subpopulations of corticocortical projection neurons in the macaque monkey visual pathways , 1996, The Journal of comparative neurology.

[23]  P. Hof,et al.  The neuropathological changes associated with normal brain aging. , 1996, Histology and histopathology.

[24]  E. Welker,et al.  Altered Sensory Processing in the Somatosensory Cortex of the Mouse Mutant Barrelless , 1996, Science.

[25]  V. Viklický,et al.  Changes of MAP2 phosphorylation during brain development. , 1995, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[26]  J. Morrison,et al.  Neurochemical phenotype of corticocortical connections in the macaque monkey: Quantitative analysis of a subset of neurofilament protein‐immunoreactive projection neurons in frontal, parietal, temporal, and cingulate cortices , 1995, The Journal of comparative neurology.

[27]  J. Morrison,et al.  Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: A quantitative immunohistochemical analysis , 1995, The Journal of comparative neurology.

[28]  M. Cynader,et al.  The correlation between cortical neuron maturation and neurofilament phosphorylation: a developmental study of phosphorylated 200 kDa neurofilament protein in cat visual cortex. , 1994, Brain research. Developmental brain research.

[29]  T. Dawson,et al.  Cellular and subcellular localization of NMDA-R1 subunit immunoreactivity in the visual cortex of adult and neonatal rats , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  J. Morrison,et al.  Alterations in neurofilament protein immunoreactivity in human hippocampal neurons related to normal aging and Alzheimer's disease , 1994, Neuroscience.

[31]  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.

[32]  J. Trojanowski,et al.  Altered Tau and Neurofilament Proteins in Neuro‐Degenerative Diseases: Diagnostic Implications for Alzheimer's Disease and Lewy Body Dementias , 1993, Brain pathology.

[33]  J. Morrison,et al.  Progressive transformation of the cytoskeleton associated with normal aging and Alzheimer's disease , 1992, Brain Research.

[34]  J. Vickers,et al.  A neurofilament protein antibody selectively labels a large ganglion cell type in the human retina , 1992, Brain Research.

[35]  D. O'Leary,et al.  Growth and targeting of subplate axons and establishment of major cortical pathways [published erratum appears in J Neurosci 1993 Mar;13(3):following table of contents] , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  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.

[37]  R. Nixon,et al.  Neurofilament phosphorylation: a new look at regulation and function , 1991, Trends in Neurosciences.

[38]  Colin Blakemore,et al.  Lack of regional specificity for connections formed between thalamus and cortex in coculture , 1991, Nature.

[39]  J. Morrison,et al.  A subpopulation of primate corticocortical neurons is distinguished by somatodendritic distribution of neurofilament protein , 1991, Brain Research.

[40]  J. Morrison,et al.  Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer's disease: II. Primary and secondary visual cortex , 1990, The Journal of comparative neurology.

[41]  Kevin Cox,et al.  Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer's disease: I. Superior frontal and inferior temporal cortex , 1990, The Journal of comparative neurology.

[42]  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.

[43]  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.

[44]  J. Morrison,et al.  Monoclonal antibody to neurofilament protein (SMI‐32) labels a subpopulation of pyramidal neurons in the human and monkey neocortex , 1989, The Journal of comparative neurology.

[45]  G. Perry,et al.  Phosphorylation of Neurofilaments Is Altered in Amyotrophic Lateral Sclerosis , 1988, Journal of neuropathology and experimental neurology.

[46]  L. Otvos,et al.  Identification of the major multiphosphorylation site in mammalian neurofilaments. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[47]  D. Perl,et al.  Accumulation of Phosphorylated Neurofilaments in Anterior Horn Motoneurons of Amyotrophic Lateral Sclerosis Patients , 1988, Journal of neuropathology and experimental neurology.

[48]  John H. Morrison,et al.  A monoclonal antibody to non-phosphorylated neurofilament protein marks the vulnerable cortical neurons in Alzheimer's disease , 1987, Brain Research.

[49]  L. Autilio‐Gambetti,et al.  Filaments of Pick's bodies contain altered cytoskeletal elements. , 1987, The American journal of pathology.

[50]  L. Sternberger,et al.  Varying degrees of phosphorylation determine microheterogeneity of the heavy neurofilament polypeptide (Nf-H) , 1987, Journal of Neuroimmunology.

[51]  A. Matus,et al.  Differential expression of distinct microtubule-associated proteins during brain development. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[52]  Charles Watson,et al.  Bregma, lambda and the interaural midpoint in stereotaxic surgery with rats of different sex, strain and weight , 1985, Journal of Neuroscience Methods.

[53]  J. Goldman,et al.  Lewy bodies of Parkinson's disease contain neurofilament antigens. , 1983, Science.

[54]  H. Killackey,et al.  Organization of corticocortical connections in the parietal cortex of the rat , 1978, The Journal of comparative neurology.

[55]  R. Lasek,et al.  The slow component of axonal transport. Identification of major structural polypeptides of the axon and their generality among mammalian neurons , 1975, The Journal of cell biology.

[56]  S. Yen,et al.  Focal accumulation of phosphorylated neurofilaments within anterior horn cell in familial amyotrophic lateral sclerosis , 2004, Acta Neuropathologica.

[57]  S. Maruyama,et al.  Immunocytochemical and ultrastructural studies of the motor cortex in amyotrophic lateral sclerosis , 2004, Acta Neuropathologica.

[58]  ichard,et al.  AXONAL TRANSECTION IN THE LESIONS OF MULTIPLE SCLEROSIS , 1998 .

[59]  B. Riederer Differential phosphorylation of MAP1b during postnatal development of the cat brain , 1995, Journal of neurocytology.

[60]  J. Kaas,et al.  Evolution of multiple areas and modules within neocortex. , 1993, Perspectives on developmental neurobiology.

[61]  M. Miller,et al.  Development of Projection and Local Circuit Neurons in Neocortex , 1988 .

[62]  K. Brodmann Vergleichende Lokalisationslehre der Großhirnrinde : in ihren Prinzipien dargestellt auf Grund des Zellenbaues , 1985 .