Map of the synapses formed with the dendrites of spiny stellate neurons of cat visual cortex

The synaptic input of six spiny stellate neurons in sublamina 4A of cat area 17 was assessed by electron microscopy. The neurons were physiologically characterized and filled with horseradish peroxidase in vivo. After processing the neurons were reconstructed at the light microscopic level using computer‐assisted methods and analyzed quantitatively. The extensive branching of the dendritic tree about 50 μm from the soma meant that the distal branches constituted five times the length of proximal dendrite. Proximal and distal portions of a single dendrite from each neuron were examined in series of ultrathin sections (1,456 sections) in the electron microscope. The majority (79%) of the 263 synapses examined were asymmetric; the remainder (21%) were symmetric. Symmetric synapses formed 35% of synapses sampled on proximal dendrites and were usually located on the shaft. They formed only 4% of synapses sampled on distal dendrites. Spines accounted for less than half of the total asymmetric synapses (45%); the remainder were on shafts. Symmetric synapses formed with four of 92 spines. Nine spines formed no synapses. Spiny stellate neurons in cat visual cortex appear to differ considerably from pyramidal neurons in having a significant asymmetric (excitatory) synaptic input to the dendritic shaft.

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

[2]  M. Colonnier Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. , 1968, Brain research.

[3]  T. Powell,et al.  Synapses on the axon hillocks and initial segments of pyramidal cell axons in the cerebral cortex. , 1969, Journal of cell science.

[4]  A. Peters,et al.  The small pyramidal neuron of the rat cerebral cortex. The perikaryon, dendrites and spines. , 1970, The American journal of anatomy.

[5]  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.

[6]  C. Gilbert,et al.  Laminar patterns of geniculocortical projection in the cat , 1976, Brain Research.

[7]  T. L. Davis,et al.  Microcircuitry of cat visual cortex: Classification of neurons in layer IV of area 17, and identification of the patterns of lateral geniculate input , 1979, The Journal of comparative neurology.

[8]  T. Powell,et al.  A qualitative and quantitative electron microscopic study of the neurons in the primate motor and somatic sensory cortices. , 1979, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[9]  E. White,et al.  Three-dimensional aspects and synaptic relationships of a Golgi-impregnated spiny stellate cell reconstructed from serial thin sections , 1980, Journal of neurocytology.

[10]  E. White,et al.  Thalamocortical synapses involving identified neurons in mouse primary somatosensory cortex: A terminal degeneration and golgi/EM study , 1981, The Journal of comparative neurology.

[11]  E. White,et al.  Thalamocortical synapses of pyramidal cells which project from SmI to MsI cortex in the mouse , 1981, The Journal of comparative neurology.

[12]  E. White,et al.  A comparison of thalamocortical and other synaptic inputs to dendrites of two non‐spiny neurons in a single barrel of mouse SmI cortex , 1981, The Journal of comparative neurology.

[13]  L. Garey,et al.  The thalamic projection to cat visual cortex: Ultrastructure of neurons identified by golgi impregnation or retrograde horseradish peroxidase transport , 1981, Neuroscience.

[14]  J. Lund,et al.  Neuronal composition and development in lamina 4C of monkey striate cortex , 1983, The Journal of comparative neurology.

[15]  P. Somogyi,et al.  Glutamate decarboxylase‐immunoreactive terminals of Golgi‐impregnated axoaxonic cells and of presumed basket cells in synaptic contact with pyramidal neurons of the cat's visual cortex , 1983, The Journal of comparative neurology.

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

[17]  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.

[18]  S. Sherman,et al.  Fine structural morphology of identified X- and Y-cells in the cat's lateral geniculate nucleus , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[19]  T. Wiesel,et al.  Patterns of synaptic input to layer 4 of cat striate cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  Daniel J. Uhlrich,et al.  Synaptic connectivity of a local circuit neurone in lateral geniculate nucleus of the cat , 1985, Nature.

[21]  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.

[22]  D. Whitteridge,et al.  Innervation of cat visual areas 17 and 18 by physiologically identified X‐ and Y‐ type thalamic afferents. II. Identification of postsynaptic targets by GABA immunocytochemistry and Golgi impregnation , 1985, The Journal of comparative neurology.

[23]  D. Whitteridge,et al.  Innervation of cat visual areas 17 and 18 by physiologically identified X‐ and Y‐ type thalamic afferents. I. Arborization patterns and quantitative distribution of postsynaptic elements , 1985, The Journal of comparative neurology.

[24]  A. Peters,et al.  The morphology and synaptic connections of spiny stellate neurons in monkey visual cortex (area 17): A golgi‐electron microscopic study , 1985, The Journal of comparative neurology.

[25]  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.

[26]  S. Brenner,et al.  The structure of the nervous system of the nematode Caenorhabditis elegans. , 1986, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[27]  P. Somogyi,et al.  Immunogold demonstration of GABA in synaptic terminals of intracellularly recorded, horseradish peroxidase-filled basket cells and clutch cells in the cat's visual cortex , 1986, Neuroscience.

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

[29]  D. Whitteridge,et al.  Connections between pyramidal neurons in layer 5 of cat visual cortex (area 17) , 1987, The Journal of comparative neurology.

[30]  D. Whitteridge,et al.  Evidence for the connections between a clutch cell and a corticotectal neuron in area 17 of the cat visual cortex , 1988, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[31]  D. Tank,et al.  Optical imaging of calcium accumulation in hippocampal pyramidal cells during synaptic activation , 1989, Nature.

[32]  D. Whitteridge,et al.  Arborisation pattern and postsynaptic targets of physiologically identified thalamocortical afferents in striate cortex of the macaque monkey , 1989, The Journal of comparative neurology.

[33]  M. J. Friedlander,et al.  Development of Y‐axon innervation of cortical area 18 in the cat. , 1989, The Journal of physiology.

[34]  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.

[35]  A. Peters,et al.  Different kinds of axon terminals forming symmetric synapses with the cell bodies and initial axon segments of layer II/III pyramidal cells. I. Morphometric analysis , 1990, Journal of neurocytology.

[36]  A. Peters,et al.  Different kinds of axon terminals forming symmetric synapses with the cell bodies and initial axon segments of layer II/III pyramidal cells. II. Synaptic junctions , 1990, Journal of neurocytology.

[37]  A. Peters The axon terminals of vasoactive intestinal polypeptide (VIP)-containing bipolar cells in rat visual cortex , 1990, Journal of neurocytology.

[38]  R. Douglas,et al.  A functional microcircuit for cat visual cortex. , 1991, The Journal of physiology.

[39]  S. B. Kater,et al.  Independent regulation of calcium revealed by imaging dendritic spines , 1991, Nature.

[40]  J. Connor,et al.  Dendritic spines as individual neuronal compartments for synaptic Ca2+ responses , 1991, Nature.

[41]  K. Martin,et al.  Excitation by geniculocortical synapses is not ‘vetoed’ at the level of dendritic spines in cat visual cortex. , 1991, The Journal of physiology.

[42]  T. Wiesel,et al.  Targets of horizontal connections in macaque primary visual cortex , 1991, The Journal of comparative neurology.

[43]  A. Peters,et al.  Different kinds of axon terminals forming symmetric synapses with the cell bodies and initial axon segments of layer II/III pyramidal cells. III. Origins and frequency of occurrence of the terminals , 1992, Journal of neurocytology.

[44]  A. Peters,et al.  Numerical relationships between geniculocortical afferents and pyramidal cell modules in cat primary visual cortex. , 1993, Cerebral cortex.

[45]  J. C. Anderson,et al.  Polyneuronal innervation of spiny stellate neurons in cat visual cortex , 1994, The Journal of comparative neurology.

[46]  J C Anderson,et al.  Synaptic output of physiologically identified spiny stellate neurons in cat visual cortex , 1994, The Journal of comparative neurology.