Expression of the L-type calcium channel in the developing mouse visual system by use of immunocytochemistry.

Developmental refinement of the retinogeniculate and retinocollicular pathways is partially dependent upon Ca(2+) channel function [J. Comp. Neurol. 440 (2001) 177-191]. We have examined the development of the L-type voltage gated Ca(2+) channel to determine if the onset of expression matches this period of refinement. Labeling by an antibody directed against the alpha 1C subunit of this channel was examined in the superior colliculus (SC), lateral geniculate nucleus (LGN), visual cortex (CTX), hippocampus (HC) and cerebellum (CB) in mice aged P3-4, P8-9, P15, P21, P28, and adults. At P3-4, labeled cells within the SC were concentrated within a dense band in the retinorecipient zone of the superficial gray layer. More lightly labeled neurons were seen in other layers. This dense band was still seen at P15, while more labeled neurons were seen in other layers. By P21-P28, labeled neurons were fairly uniformly distributed throughout all layers of SC. Neuronal cell types appeared to be labeled at all ages examined within the LGN. Within CTX, putative layer V-VI pyramidal neurons were well labeled at P4 and later ages, and labeled layer II-III pyramids could be distinguished by P9 and later ages. The dendrites and cell bodies of pyramidal neurons within CA1-CA3 of HC, granule neurons in the dentate gyrus, and Purkinje neurons in CB were labeled at all ages examined. We conclude that the L-type Ca(2+) channel is expressed in many neurons within retinorecipient targets as well as in other brain regions during the developmental period in which pathway refinement and synaptic plasticity occurs.

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

[2]  W. Abraham,et al.  L-type voltage-sensitive calcium channel antagonists block heterosynaptic long-term depression in the dentate gyrus of anaesthetized rats , 1994, Neuroscience Letters.

[3]  F. Lo,et al.  Nitric oxide, impulse activity, and neurotrophins in visual system development 1 1 Published on the World Wide Web on 16 August 2000. , 2000, Brain Research.

[4]  A. Burkhalter,et al.  Differential expression of voltage-gated calcium channels in identified visual cortical neurons , 1991, Neuron.

[5]  R. Mize,et al.  The role of nitric oxide in development of the patch-cluster system and retinocollicular pathways in the rodent superior colliculus. , 1998, Progress in brain research.

[6]  J. Hell,et al.  Molecular cloning of the alpha-1 subunit of an omega-conotoxin-sensitive calcium channel. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[7]  R. Guillery,et al.  The early development of retinal ganglion cells with uncrossed axons in the mouse: retinal position and axonal course. , 1990, Development.

[8]  P. Ince,et al.  The expression of voltage-dependent calcium channel beta subunits in human cerebellum , 1997, Neuroscience.

[9]  Jeffery R. Wickens,et al.  The involvement of L-type calcium channels in heterosynaptic long-term depression in the hippocampus , 1991, Neuroscience Letters.

[10]  G. Jeffery,et al.  Retinal ganglion cell death and terminal field retraction in the developing rodent visual system. , 1984, Brain research.

[11]  Daniel E Feldman,et al.  Long-Term Depression at Thalamocortical Synapses in Developing Rat Somatosensory Cortex , 1998, Neuron.

[12]  F. Lo,et al.  Synaptic Regulation of L-Type Ca2+ Channel Activity and Long-Term Depression during Refinement of the Retinocollicular Pathway in Developing Rodent Superior Colliculus , 2000, The Journal of Neuroscience.

[13]  C. Shatz,et al.  Developmental mechanisms that generate precise patterns of neuronal connectivity , 1993, Cell.

[14]  G. Elston,et al.  Pyramidal Cells, Patches, and Cortical Columns: a Comparative Study of Infragranular Neurons in TEO, TE, and the Superior Temporal Polysensory Area of the Macaque Monkey , 2000, The Journal of Neuroscience.

[15]  A. Bacci,et al.  Different localizations and functions of L-type and N-type calcium channels during development of hippocampal neurons. , 2000, Developmental biology.

[16]  K. Campbell,et al.  Identification of Three Subunits of the High Affinity ω-Conotoxin MVIIC-sensitive Ca2+ Channel* , 1996, The Journal of Biological Chemistry.

[17]  Alessandra Angelucci,et al.  A Role for Nitric Oxide in the Development of the Ferret Retinogeniculate Projection , 1996, The Journal of Neuroscience.

[18]  R. Lund,et al.  Development of the rat's uncrossed retinotectal pathway and its relation to plasticity studies. , 1979, Science.

[19]  P. Ince,et al.  Distribution ofα1A, α1B andα1E voltage-dependent calcium channel subunits in the human hippocampus and parahippocampal gyrus , 1996, Neuroscience.

[20]  William A. Catterall,et al.  Clustering of L-type Ca2+ channels at the base of major dendrites in hippocampal pyramidal neurons , 1990, Nature.

[21]  M. Sur,et al.  Disruption of retinogeniculate afferent segregation by antagonists to NMDA receptors , 1991, Nature.

[22]  J. G. Netzeband,et al.  L-Type Calcium Channels Mediate Calcium Oscillations in Early Postnatal Purkinje Neurons , 2000, The Journal of Neuroscience.

[23]  D. Johnston,et al.  Contribution of voltage-gated Ca2+ channels to homosynaptic long-term depression in the CA1 region in vitro. , 1997, Journal of neurophysiology.

[24]  P. Huang,et al.  Refinement of the ipsilateral retinocollicular projection is disrupted in double endothelial and neuronal nitric oxide synthase gene knockout mice. , 2000, Brain research. Developmental brain research.

[25]  J. Priestley,et al.  Distribution of the voltage‐dependent calcium channel α1A subunit throughout the mature rat brain and its relationship to neurotransmitter pathways , 1998 .

[26]  S C McLoon,et al.  NMDA Receptor-Mediated Refinement of a Transient Retinotectal Projection during Development Requires Nitric Oxide , 1999, The Journal of Neuroscience.

[27]  R. Brownstone,et al.  Development of L‐type calcium channels and a nifedipine‐sensitive motor activity in the postnatal mouse spinal cord , 1999, The European journal of neuroscience.

[28]  R. Tsien,et al.  Targeted disruption of the Ca2+ channel beta3 subunit reduces N- and L-type Ca2+ channel activity and alters the voltage-dependent activation of P/Q-type Ca2+ channels in neurons. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[29]  J. Parnavelas,et al.  The development of excitatory transmitter amino acid-containing neurons in the rat visual cortex , 1996, Experimental Brain Research.

[30]  H. López,et al.  δ Opioid Receptor Modulation of Several Voltage-Dependent Ca2+ Currents in Rat Sensory Neurons , 1999, The Journal of Neuroscience.

[31]  R. Mize,et al.  Normal development of the ipsilateral retinocollicular pathway and its disruption in double endothelial and neuronal nitric oxide synthase gene knockout mice , 2000, The Journal of comparative neurology.

[32]  M. Constantine-Paton,et al.  N-methyl-D-aspartate receptor antagonists disrupt the formation of a mammalian neural map. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[33]  J. Hell,et al.  Differential phosphorylation of two size forms of the neuronal class C L-type calcium channel alpha 1 subunit. , 1993, The Journal of biological chemistry.

[34]  M. Weiergräber,et al.  Immunohistochemical detection of alpha1E voltage-gated Ca(2+) channel isoforms in cerebellum, INS-1 cells, and neuroendocrine cells of the digestive system. , 1999, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[35]  Y. Namkung,et al.  Development of the visual pathway is disrupted in mice with a targeted disruption of the calcium channel β3‐subunit gene , 2001, The Journal of comparative neurology.

[36]  G. Gallo,et al.  Stabilization of Growing Retinal Axons by the Combined Signaling of Nitric Oxide and Brain-Derived Neurotrophic Factor , 2000, The Journal of Neuroscience.

[37]  J. Hell,et al.  Identification and differential subcellular localization of the neuronal class C and class D L-type calcium channel alpha 1 subunits , 1993, The Journal of cell biology.

[38]  George Paxinos,et al.  The Mouse Brain in Stereotaxic Coordinates , 2001 .

[39]  J. Hell,et al.  Immunochemical identification and subcellular distribution of the alpha 1A subunits of brain calcium channels , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  J. Fawcett,et al.  Regressive events in neurogenesis. , 1984, Science.

[41]  S C McLoon,et al.  Involvement of nitric oxide in the elimination of a transient retinotectal projection in development. , 1994, Science.

[42]  W. Catterall,et al.  Subunit structure and localization of dihydropyridine-sensitive calcium channels in mammalian brain, spinal cord, and retina , 1990, Neuron.

[44]  D. O'Leary,et al.  Development of topographic order in the mammalian retinocollicular projection , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  M. Sur,et al.  Nitric oxide as a signaling molecule in visual system development. , 1998, Progress in brain research.

[46]  G. Schneider,et al.  Development of the crossed retinocollicular projection in the mouse , 1986, The Journal of comparative neurology.

[47]  M Imbert,et al.  Prenatal and postnatal development of retinogeniculate and retinocollicular projections in the mouse , 1984, The Journal of comparative neurology.