Intracellularly labeled pyramidal neurons in the cortical areas projecting to the spinal cord I. Electrophysiological properties of pyramidal neurons

To study cortical motor control, we examined electrical characteristics of pyramidal neurons in the present report, and intra- or juxta-columnar connections of the pyramidal neurons to corticospinal neurons in the accompanying report. Pyramidal neurons were intracellularly recorded and stained in slices of rat motorsensory cortices (areas FL, HL and M1) where many corticospinal neurons were labeled retrogradely. They were morphologically classified into classical, star and other modified pyramidal neurons, and electrophysiologically into regular-spiking (RS), intrinsic bursting (IB) and irregular-spiking (IS) neurons on the basis of spiking pattern in response to 500 ms depolarizing current pulses. RS responses were further divided into RS with slow adaptation (RS-SA) and RS with fast adaptation (RS-FA). The electrical properties were associated with the laminar location of the neurons; RS-SA responses were observed frequently in layer II/III and less frequently in layers IV-VI, and IB and IS responses were exclusively found in layers V and VI, respectively. Interestingly, all layer IV neurons in area FL/HL were RS-FA star-pyramidal neurons, whereas layer IV neurons in area M1 were RS-SA classical pyramidal neurons. Although weak stimulation of areas FL/HL and M1 is known to elicit movement, these results suggest different information processings between the two areas.

[1]  J. Eccles.  The Cerebral Neocortex , 1984 .

[2]  J. Nerbonne,et al.  Role of voltage-gated K+ currents in mediating the regular-spiking phenotype of callosal-projecting rat visual cortical neurons. , 1997, Journal of neurophysiology.

[3]  H. Pockberger,et al.  Electrophysiological and morphological properties of rat motor cortex neurons in vivo , 1991, Brain Research.

[4]  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.

[5]  E. G. Jones,et al.  Varieties and distribution of non‐pyramidal cells in the somatic sensory cortex of the squirrel monkey , 1975, The Journal of comparative neurology.

[6]  H. Asanuma,et al.  Patterns of contraction of distal forelimb muscles produced by intracortical stimulation in cats. , 1971, Brain research.

[7]  T. Kaneko,et al.  Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67‐GFP knock‐in mouse , 2003, The Journal of comparative neurology.

[8]  T. Kaneko,et al.  Glutaminase-positive and glutaminase-negative pyramidal cells in layer VI of the primary motor and somatosensory cortices: a combined analysis by intracellular staining and immunocytochemistry in the rat , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  T. Kaneko,et al.  Spiny stellate neurones in layer VI of the rat cerebral cortex. , 1996, Neuroreport.

[10]  D. Simons,et al.  Morphology of Golgi‐Cox‐impregnated barrel neurons in rat SmI cortex , 1984, The Journal of comparative neurology.

[11]  S. Levay,et al.  Synaptic patterns in the visual cortex of the cat and monkey. Electron microscopy of Golgi Preparations , 1973, The Journal of comparative neurology.

[12]  Takeshi Kaneko,et al.  Intracellularly labeled pyramidal neurons in the cortical areas projecting to the spinal cord II. Intra- and juxta-columnar projection of pyramidal neurons to corticospinal neurons , 2004, Neuroscience Research.

[13]  R. Kötter,et al.  Layer-Specific Intracolumnar and Transcolumnar Functional Connectivity of Layer V Pyramidal Cells in Rat Barrel Cortex , 2001, The Journal of Neuroscience.

[14]  J. Lübke,et al.  Columnar Organization of Dendrites and Axons of Single and Synaptically Coupled Excitatory Spiny Neurons in Layer 4 of the Rat Barrel Cortex , 2000, The Journal of Neuroscience.

[15]  F. Ebner,et al.  Evidence for two organizational plans within the somatic sensory‐motor cortex of the rat , 1979, The Journal of comparative neurology.

[16]  F. Fujiyama,et al.  Immunohistochemical localization of candidates for vesicular glutamate transporters in the rat brain , 2002, The Journal of comparative neurology.

[17]  L. L. Porter,et al.  Organization and synaptic relationships of the projection from the primary sensory to the primary motor cortex in the cat , 1988, The Journal of comparative neurology.

[18]  D. Simons,et al.  Spatial organization of thalamocortical and corticothalamic projection systems in the rat SmI barrel cortex , 1989, The Journal of comparative neurology.

[19]  R. Hall,et al.  Organization of motor and somatosensory neocortex in the albino rat , 1974 .

[20]  S. Wise,et al.  The motor cortex of the rat: Cytoarchitecture and microstimulation mapping , 1982, The Journal of comparative neurology.

[21]  Leonard D. Aldes,et al.  Thalamic connectivity of rat somatic motor cortex , 1988, Brain Research Bulletin.

[22]  J. Winer,et al.  Layer VI in cat primary auditory cortex: Golgi study and sublaminar origins of projection neurons , 1999, The Journal of comparative neurology.

[23]  M. Miller,et al.  The origin of corticospinal projection neurons in rat , 2004, Experimental Brain Research.

[24]  H Asanuma,et al.  Information processing within the motor cortex. I. Responses of morphologically identified motor cortical cells to stimulation of the somatosensor cortex , 1994, The Journal of comparative neurology.

[25]  A. Keller,et al.  Intrinsic circuitry and physiological properties of pyramidal neurons in rat barrel cortex , 1997, Experimental Brain Research.

[26]  J. Nerbonne,et al.  Three kinetically distinct Ca2+-independent depolarization-activated K+ currents in callosal-projecting rat visual cortical neurons. , 1997, Journal of neurophysiology.

[27]  V. Mountcastle.  The columnar organization of the neocortex. , 1997, Brain : a journal of neurology.

[28]  Gray Eg.  Axo-somatic and axo-dendritic synapses of the cerebral cortex: An electron microscope study , 1959 .

[29]  T. Powell,et al.  An electron microscopic study of the types and proportions of neurons in the cortex of the motor and visual areas of the cat and rat. , 1980, Brain : a journal of neurology.

[30]  Alexander M Binshtok,et al.  Functionally Distinct NMDA Receptors Mediate Horizontal Connectivity within Layer 4 of Mouse Barrel Cortex , 1998, Neuron.

[31]  Takeshi Kaneko,et al.  Improved retrograde axonal transport and subsequent visualization of tetramethylrhodamine (TMR)-dextran amine by means of an acidic injection vehicle and antibodies against TMR , 1996, Journal of Neuroscience Methods.

[32]  T. Woolsey,et al.  Structure of layer IV in the somatosensory neocortex of the rat: Description and comparison with the mouse , 1974, The Journal of comparative neurology.

[33]  A Keller,et al.  Intrinsic synaptic organization of the motor cortex. , 1993, Cerebral cortex.

[34]  J. Lübke,et al.  Reliable synaptic connections between pairs of excitatory layer 4 neurones within a single ‘barrel’ of developing rat somatosensory cortex , 1999, The Journal of physiology.

[35]  J F Fulton,et al.  Physiology of the Nervous System , 1939, Science.

[36]  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.

[37]  R. Silver,et al.  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 , 2002, The Journal of physiology.

[38]  F. Karube,et al.  Axon Branching and Synaptic Bouton Phenotypes in GABAergic Nonpyramidal Cell Subtypes , 2004, The Journal of Neuroscience.

[39]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[40]  H. Asanuma,et al.  Topographical organization of cortical efferent zones projecting to distal forelimb muscles in the monkey , 2004, Experimental Brain Research.

[41]  J. Lund.  Organization of neurons in the visual cortex, area 17, of the monkey (Macaca mulatta) , 1973, The Journal of comparative neurology.

[42]  B. Connors,et al.  Correlation between intrinsic firing patterns and thalamocortical synaptic responses of neurons in mouse barrel cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  S. Kakei,et al.  Distribution of terminals of thalamocortical fibers originating from the ventrolateral nucleus of the cat thalamus , 1989, Neuroscience Letters.

[44]  Idan Segev,et al.  Compartmental models of complex neurons , 1989 .

[45]  E. Galarraga,et al.  Different Ca2+ source for slow AHP in completely adapting and repetitive firing pyramidal neurons. , 1999, Neuroreport.

[46]  R. Pascher,et al.  Aspects of the quantitative analysis of neurons in the cerebral cortex , 1996, Journal of Neuroscience Methods.

[47]  D. F. Wann,et al.  Mouse SmI cortex: qualitative and quantitative classification of golgi-impregnated barrel neurons. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[48]  V. Mountcastle.  Modality and topographic properties of single neurons of cat's somatic sensory cortex. , 1957, Journal of neurophysiology.

[49]  M Steriade,et al.  Electrophysiology of cat association cortical cells in vivo: intrinsic properties and synaptic responses. , 1993, Journal of neurophysiology.

[50]  D. Oertel,et al.  Encoding of Timing in the Brain Stem Auditory Nuclei of Vertebrates , 1997, Neuron.

[51]  J. A. Hirsch.  Synaptic integration in layer IV of the ferret striate cortex. , 1995, The Journal of physiology.

[52]  J. O'leary,et al.  Structure of the area striata of the cat , 1941 .

[53]  M. Wiesendanger,et al.  Corticomotoneuronal connections in the rat: Evidence from double‐labeling of motoneurons and corticospinal axon arborizations , 1991, The Journal of comparative neurology.

[54]  A. Scheibel,et al.  Pattern and field in cortical structure: The rabbit , 1967, The Journal of comparative neurology.

[55]  G. Henry,et al.  Anatomical organization of the primary visual cortex (area 17) of the cat. A comparison with area 17 of the macaque monkey , 1979, The Journal of comparative neurology.

[56]  R. Metherate,et al.  Intrinsic electrophysiology of neurons in thalamorecipient layers of developing rat auditory cortex. , 1999, Brain research. Developmental brain research.

[57]  J. Lund,et al.  Anatomical organization of primate visual cortex area VII , 1981, The Journal of comparative neurology.

[58]  Karl Zilles,et al.  Functional diversity of layer IV spiny neurons in rat somatosensory cortex: quantitative morphology of electrophysiologically characterized and biocytin labeled cells. , 2004, Cerebral cortex.

[59]  G. Meyer,et al.  The spiny stellate neurons in layer IV of the human auditory cortex. A Golgi study , 1989, Neuroscience.

[60]  F. Fujiyama,et al.  Immunocytochemical localization of candidates for vesicular glutamate transporters in the rat cerebral cortex , 2001, The Journal of comparative neurology.

[61]  B. Connors,et al.  Intrinsic firing patterns of diverse neocortical neurons , 1990, Trends in Neurosciences.

[62]  A. Peters,et al.  The neuronal composition of area 17 of rat visual cortex. I. The pyramidal cells , 1985, The Journal of comparative neurology.

[63]  C H Berthold,et al.  The existence of a layer IV in the rat motor cortex. , 1997, Cerebral cortex.

[64]  H Asanuma,et al.  Information processing within the motor cortex. II. Intracortical connections between neurons receiving somatosensory cortical input and motor output neurons of the cortex , 1994, The Journal of comparative neurology.

[65]  Y. Kang,et al.  Electrophysiological and morphological characteristics of layer VI pyramidal cells in the cat motor cortex. , 1994, Journal of neurophysiology.

[66]  A. Laverghetta,et al.  Differential morphology of pyramidal tract‐type and intratelencephalically projecting‐type corticostriatal neurons and their intrastriatal terminals in rats , 2003, The Journal of comparative neurology.

[67]  D. Whitteridge,et al.  Form, function and intracortical projections of spiny neurones in the striate visual cortex of the cat. , 1984, The Journal of physiology.

[68]  R. Yuste,et al.  Thalamocortical Bursts Trigger Recurrent Activity in Neocortical Networks: Layer 4 as a Frequency-Dependent Gate , 2002, The Journal of Neuroscience.

[69]  Prof. Dr. Karl Zilles.  The Cortex of the Rat , 1985, Springer Berlin Heidelberg.

[70]  T. Kosaka,et al.  Quantitative analysis of neurons and glial cells in the rat somatosensory cortex, with special reference to GABAergic neurons and parvalbumin-containing neurons , 2004, Experimental Brain Research.

[71]  P. B. Cipolloni,et al.  Golgi, histochemical, and immunocytochemical analyses of the neurons of auditory-related cortices of the rhesus monkey , 1991, Experimental Neurology.

[72]  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.

[73]  Yves Gioanni,et al.  Electrophysiological properties of pyramidal neurons in the rat prefrontal cortex: an in vivo intracellular recording study. , 2002, Cerebral cortex.

[74]  B. Sakmann,et al.  The Excitatory Neuronal Network of Rat Layer 4 Barrel Cortex , 2000, The Journal of Neuroscience.

[75]  T. Kaneko,et al.  Predominant information transfer from layer III pyramidal neurons to corticospinal neurons , 2000, The Journal of comparative neurology.