Morphological properties of intracellularly labeled layer I neurons in rat neocortex

The morphology of neurons in layer I of rat neocortex, including Cajal‐Retzius (CR) cells, was studied by using intracellular biocytin staining in brain slices obtained from rats during the first 22 postnatal days. Within the first postnatal week, horizontal bipolar neurons or CR cells were prominent in layer I. Typically, CR cells had one main dendrite and one axon originating from opposite poles of the somata. Even though the main dendrites and axons could be quite long, complex dendritic or axonal arbors were not observed. Starting around postnatal day 6 (PN 6), CR cells were less frequently observed. From PN 10 to PN 21, nonpyramidal neurons with diverse morphologies became the main neuronal component in layer I. The somata of layer I nonpyramidal neurons were quite variable in size and shape. Dendrites were smooth or sparsely spiny, and the dendritic trees were mainly restricted to layer I, covering an area with a diameter of about 200 μm. Axon collaterals of these cells formed elaborate arbors with diameters of around 700 μm in layer I and extending, in many cases, to layer II/III and even layer IV. This extensive axonal plexus provides a rich anatomical base on which layer I neurons, functioning as local circuit elements, may interact with each other and with neurons in other layers. © 1996 Wiley‐Liss, Inc.

[1]  J. Parnavelas,et al.  Retzius-Cajal cells: an ultrastructural study in the developing visual cortex of the rat , 1982, Journal of neurocytology.

[2]  F. Zhou,et al.  Layer I neurons of rat neocortex. I. Action potential and repetitive firing properties. , 1996, Journal of neurophysiology.

[3]  J. Winer,et al.  Laminar distribution and neuronal targets of GABAergic axon terminals in cat primary auditory cortex (AI) , 1994, The Journal of comparative neurology.

[4]  J. Parnavelas,et al.  Further evidence that Retzius-Cajal cells transform to nonpyramidal neurons in the developing rat visual cortex , 1983, Journal of neurocytology.

[5]  A. Peters,et al.  A three dimensional study of layer I of the rat parietal cortex , 1973, The Journal of comparative neurology.

[6]  B Sakmann,et al.  Detailed passive cable models of whole-cell recorded CA3 pyramidal neurons in rat hippocampal slices , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  George Paxinos,et al.  Atlas Of The Developing Rat Brain , 1991 .

[8]  P. Somogyi,et al.  Evidence for interlaminar inhibitory circuits in the striate cortex of the cat , 1987, The Journal of comparative neurology.

[9]  M. Seike,et al.  The reeler gene-associated antigen on cajal-retzius neurons is a crucial molecule for laminar organization of cortical neurons , 1995, Neuron.

[10]  K. Horikawa,et al.  A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates , 1988, Journal of Neuroscience Methods.

[11]  H. Schwark,et al.  Distribution and proportions of GABA‐Immunoreactive neurons in cat primary somatosensory cortex , 1994, The Journal of comparative neurology.

[12]  J. Deuchars,et al.  Innervation of burst firing spiny interneurons by pyramidal cells in deep layers of rat somatomotor cortex: Paired intracellular recordings with biocytin filling , 1995, Neuroscience.

[13]  G. Meyer,et al.  Developmental changes in layer I of the human neocortex during prenatal life: A DiI‐tracing and AChE and NADPH‐d histochemistry study , 1993, The Journal of comparative neurology.

[14]  P. Derer,et al.  Cajal-retzius cell ontogenesis and death in mouse brain visualized with horseradish peroxidase and electron microscopy , 1990, Neuroscience.

[15]  M. Marín‐Padilla,et al.  Early Ontogenesis of the Human Cerebral Cortex , 1988 .

[16]  A. Lieberman,et al.  Neurons in layer I of the developing occipital cortex of the rat , 1977, The Journal of comparative neurology.

[17]  F. Zhou,et al.  Layer I neurons of the rat neocortex. II. Voltage-dependent outward currents. , 1996, Journal of neurophysiology.

[18]  C. Wilson,et al.  Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex. , 1994, Journal of neurophysiology.

[19]  J. Winer,et al.  Morphology and spatial distribution of GABAergic neurons in cat primary auditory cortex (AI) , 1994, The Journal of comparative neurology.

[20]  M Marín-Padilla,et al.  Three‐dimensional structural organization of layer I of the human cerebral cortex: A golgi study , 1990, The Journal of comparative neurology.

[21]  G. Meyer,et al.  Postnatal maturation of nonpyramidal neurons in the visual cortex of the cat , 1984, The Journal of comparative neurology.

[22]  J. D. del Río,et al.  Glutamate-like immunoreactivity and fate of Cajal-Retzius cells in the murine cortex as identified with calretinin antibody. , 1995, Cerebral cortex.

[23]  H. Uylings,et al.  Postnatal volumetric development of the prefrontal cortex in the rat , 1985, The Journal of comparative neurology.

[24]  Y. Kubota,et al.  Physiological and morphological identification of somatostatin- or vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  P. Somogyi,et al.  Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat , 1983, Neuroscience.

[26]  J. Winer,et al.  Populations of GABAergic neurons and axons in layer I of rat auditory cortex , 1989, Neuroscience.

[27]  K. Rockland,et al.  Terminal arbors of individual “Feedback” axons projecting from area V2 to V1 in the macaque monkey: A study using immunohistochemistry of anterogradely transported Phaseolus vulgaris‐leucoagglutinin , 1989, The Journal of comparative neurology.

[28]  C. Noback,et al.  Postnatal ontogenesis of neurons in cat neocortex , 1961, The Journal of comparative neurology.

[29]  D. Whitteridge,et al.  Synaptic connections of intracellularly filled clutch cells: A type of small basket cell in the visual cortex of the cat , 1985, The Journal of comparative neurology.

[30]  N. Spruston,et al.  Voltage- and space-clamp errors associated with the measurement of electrotonically remote synaptic events. , 1993, Journal of neurophysiology.

[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]  S. Cajal Cajal on the cerebral cortex , 1988 .

[33]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[34]  P. Somogyi,et al.  A High Degree of Spatial Selectivity in the Axonal and Dendritic Domains of Physiologically Identified Local‐circuit Neurons in the Dentate Gyms of the Rat Hippocampus , 1993, The European journal of neuroscience.

[35]  JJ Hablitz,et al.  Postnatal development of membrane properties of layer I neurons in rat neocortex , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  M Marín-Padilla,et al.  Ontogenesis of the pyramidal cell of the mammalian neocortex and developmental cytoarchitectonics: A unifying theory , 1992, The Journal of comparative neurology.

[37]  K. Imamoto,et al.  Cajal-Retzius neurons identified by GABA immunohistochemistry in layer I of the rat cerebral cortex , 1994, Neuroscience Research.

[38]  L. Haberly Structure of the piriform cortex of the opossum. I. Description of neuron types with golgi methods , 1983, The Journal of comparative neurology.

[39]  Kevan A. C. Martin,et al.  The neurons in layer 1 of cat visual cortex , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[40]  M. J. Friedlander,et al.  Physiological, morphological, and cytochemical characteristics of a layer 1 neuron in cat striate cortex , 1989, The Journal of comparative neurology.

[41]  C. Beaulieu,et al.  Quantitative aspects of the GABA circuitry in the primary visual cortex of the adult rat , 1994, The Journal of comparative neurology.

[42]  Y. Kawaguchi,et al.  Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. , 1993, Journal of neurophysiology.

[43]  M. Paula-Barbosa,et al.  A golgi and electron microscopical study of nerve cells in layer I of the cat auditory cortex , 1975, Brain Research.

[44]  M. Colonnier,et al.  A laminar analysis of the number of round‐asymmetrical and flat‐symmetrical synapses on spines, dendritic trunks, and cell bodies in area 17 of the cat , 1985, The Journal of comparative neurology.

[45]  Rafael Yuste,et al.  Ca2+ accumulations in dendrites of neocortical pyramidal neurons: An apical band and evidence for two functional compartments , 1994, Neuron.

[46]  G M Shepherd,et al.  Electrotonic structure of olfactory sensory neurons analyzed by intracellular and whole cell patch techniques. , 1991, Journal of neurophysiology.