Physiology and morphology of callosal projection neurons in mouse

In the mammalian neocortex, the corpus callosum serves as the major source of interhemispheric communication, composed of axons from callosal neurons located in supragranular (II/III) and infragranular (V/VI) layers. We sought to characterize the physiology and morphology of supragranular and infragranular callosal neurons in mice using retrograde tracers and whole-cell patch clamp recordings. Whole-cell patch clamp recordings were made from retrogradely labeled callosal neurons following unilateral injection of fluorescent latex microspheres in the contralateral sensory-motor cortex. Following recordings and biocytin dialysis, labeled neurons were reconstructed using computer-assisted camera lucida (Neurolucida) for morphological analyses. Whole-cell recordings revealed that callosal neurons in both supra- and infragranular layers display very similar intrinsic membrane properties and are characteristic regular-spiking neurons. Morphological features examined from biocytin-filled reconstructions as well as retrogradely BDA labeled cells did not reveal any differences. Analysis of spontaneous postsynaptic potentials from callosal neurons did reveal several differences including average amplitude, frequency, and decay time. These findings suggest that callosal neurons in both supra- and infragranular layers have similar phenotypes though belong to different local, intracortical networks.

[1]  B. Connors,et al.  Electrophysiological properties of neocortical neurons in vitro. , 1982, Journal of neurophysiology.

[2]  S. Nelson,et al.  Probing the transcriptome of neuronal cell types , 2006, Current Opinion in Neurobiology.

[3]  E. White.  Cortical Circuits: Synaptic Organization of the Cerebral Cortex , 1989 .

[4]  C. Blakemore,et al.  Pyramidal neurons in layer 5 of the rat visual cortex. I. Correlation among cell morphology, intrinsic electrophysiological properties, and axon targets , 1994, The Journal of comparative neurology.

[5]  H. Swadlow.  Efferent neurons and suspected interneurons in S-1 forelimb representation of the awake rabbit: receptive fields and axonal properties. , 1990, Journal of neurophysiology.

[6]  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.

[7]  Matthias Schmidt,et al.  Correlation of electrophysiology, morphology, and functions in corticotectal and corticopretectal projection neurons in rat visual cortex , 1998, Experimental Brain Research.

[8]  S P Wise,et al.  Developmental studies of thalamocortical and commissural connections in the rat somatic sensory cortex , 1978, The Journal of comparative neurology.

[9]  J. DeFelipe,et al.  Microstructure of the neocortex: Comparative aspects , 2002, Journal of neurocytology.

[10]  J. Seamans,et al.  Electrophysiological and morphological properties of layers V-VI principal pyramidal cells in rat prefrontal cortex in vitro , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  Joshua C. Brumberg,et al.  The sensorimotor slice , 2007, Journal of Neuroscience Methods.

[12]  Serge Charpak,et al.  Two populations of layer v pyramidal cells of the mouse neocortex: development and sensitivity to anesthetics. , 2005, Journal of neurophysiology.

[13]  H. Markram,et al.  Morphological, Electrophysiological, and Synaptic Properties of Corticocallosal Pyramidal Cells in the Neonatal Rat Neocortex , 2006 .

[14]  Maria V. Sanchez-Vives,et al.  Slow adaptation in fast-spiking neurons of visual cortex. , 2005, Journal of neurophysiology.

[15]  M. Marín‐Padilla,et al.  Neocortical Development , 1992, Journal of Cognitive Neuroscience.

[16]  M. L. Pucak,et al.  Dendritic morphology of callosal and ipsilateral projection neurons in monkey prefrontal cortex , 2002, Neuroscience.

[17]  R. R. Sturrock,et al.  Problems of the Keimbahn: New Work on Mammalian Germ Cell Lineage , 1985 .

[18]  S. Nelson,et al.  Molecular taxonomy of major neuronal classes in the adult mouse forebrain , 2006, Nature Neuroscience.

[19]  K. Svoboda,et al.  Channelrhodopsin-2–assisted circuit mapping of long-range callosal projections , 2007, Nature Neuroscience.

[20]  F. Ebner,et al.  Lesions of Mature Barrel Field Cortex Interfere with Sensory Processing and Plasticity in Connected Areas of the Contralateral Hemisphere , 2003, The Journal of Neuroscience.

[21]  W. Cowan,et al.  Evidence that the early postnatal restriction of the cells of origin of the callosal projection is due to the elimination of axonal collaterals rather than to the death of neurons. , 1981, Brain research.

[22]  J. D. Macklis,et al.  Large‐scale maintenance of dual projections by callosal and frontal cortical projection neurons in adult mice , 2005, The Journal of comparative neurology.

[23]  M. Fabri,et al.  Glutamic acid decarboxylase immunoreactivity in callosal projecting neurons of cat and rat somatic sensory areas , 2004, Neuroscience.

[24]  N T Carnevale,et al.  Electrotonic architecture of hippocampal CA1 pyramidal neurons based on three-dimensional reconstructions. , 1996, Journal of neurophysiology.

[25]  F. Ebner,et al.  Chronic suppression of activity in barrel field cortex downregulates sensory responses in contralateral barrel field cortex. , 2005, Journal of neurophysiology.

[26]  M. Gazzaniga.  Forty-five years of split-brain research and still going strong , 2005, Nature Reviews Neuroscience.

[27]  Y. Gonchar,et al.  GABA-immunopositive neurons in rat neocortex with contralateral projections to S-I , 1995, Brain Research.

[28]  S. Nelson,et al.  Layer V neurons in mouse cortex projecting to different targets have distinct physiological properties. , 2007, Journal of neurophysiology.

[29]  F. Clascá,et al.  Embryonic and postnatal development of the layer I-directed ("matrix") thalamocortical system in the rat. , 2008, Cerebral cortex.

[30]  L. Roux,et al.  Morphological and Physiological Characterization of Layer VI Corticofugal Neurons of Mouse Primary Visual Cortex , 2003 .

[31]  D. McCormick,et al.  Ionic Mechanisms Underlying Repetitive High-Frequency Burst Firing in Supragranular Cortical Neurons , 2000, The Journal of Neuroscience.

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

[33]  H. Killackey,et al.  Variability in the distribution of callosal projection neurons in the adult rat parietal cortex , 1984, Brain Research.

[34]  S. Nelson,et al.  The problem of neuronal cell types: a physiological genomics approach , 2006, Trends in Neurosciences.

[35]  D. McCormick,et al.  Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. , 1985, Journal of neurophysiology.

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

[37]  E. G. Jones,et al.  The organization and postnatal development of the commissural projection of the rat somatic sensory cortex , 1976, The Journal of comparative neurology.

[38]  M. Steriade,et al.  Electrophysiological properties and input-output organization of callosal neurons in cat association cortex. , 2003, Journal of neurophysiology.

[39]  Z. Molnár,et al.  Towards the classification of subpopulations of layer V pyramidal projection neurons , 2006, Neuroscience Research.

[40]  H. Swadlow.  Efferent neurons and suspected interneurons in S-1 vibrissa cortex of the awake rabbit: receptive fields and axonal properties. , 1989, Journal of neurophysiology.

[41]  H. Markram,et al.  Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. , 1997, The Journal of physiology.

[42]  A. Reeves,et al.  Total Corpus Callosotomy for Control of Medically Intractable Epilepsy , 1985 .

[43]  M Steriade,et al.  Synaptic responsiveness of neocortical neurons to callosal volleys during paroxysmal depolarizing shifts , 2004, Neuroscience.

[44]  J. C Brumberg.  Firing pattern modulation by oscillatory input in supragranular pyramidal neurons , 2002, Neuroscience.

[45]  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.

[46]  Nace L. Golding,et al.  Compartmental Models Simulating a Dichotomy of Action Potential Backpropagation in Ca1 Pyramidal Neuron Dendrites , 2001, Journal of neurophysiology.

[47]  H. Markram.  A network of tufted layer 5 pyramidal neurons. , 1997, Cerebral cortex.

[48]  R Kötter,et al.  Morphology, electrophysiology and functional input connectivity of pyramidal neurons characterizes a genuine layer va in the primary somatosensory cortex. , 2006, Cerebral cortex.

[49]  Miguel A L Nicolelis,et al.  Heterogeneous integration of bilateral whisker signals by neurons in primary somatosensory cortex of awake rats. , 2005, Journal of neurophysiology.

[50]  Marco Capogna,et al.  GABAergic and pyramidal neurons of deep cortical layers directly receive and differently integrate callosal input. , 2007, Cerebral cortex.

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

[52]  R. Yuste,et al.  Morphological and physiological characterization of layer VI corticofugal neurons of mouse primary visual cortex. , 2003, Journal of neurophysiology.