Microcircuitry of bipolar cells in cat retina

We have studied 15 bipolar neurons from a small patch (14 X 120 micron) of adult cat retina located within the area centralis. From electron micrographs of 189 serial ultrathin sections, the axon of each bipolar cell was substantially reconstructed with its synaptic inputs and outputs by means of a computer-controlled reconstruction system. Based on differences in stratification, cytology, and synaptic connections, we identified eight different cell types among the group of 15 neurons: one type of rod bipolar and seven types of cone bipolar neurons. These types correspond to those identified by the Golgi method and by intracellular recording. Those bipolar cell types for which we reconstructed three or four examples were extremely regular in form, size, and cytology, and also in the quantitative details of their synaptic connections. They appeared quite as specific in these respects as invertebrate “identified” neurons. The synaptic patterns observed for each type of bipolar neuron were complex but may be summarized as follows: the rod bipolar axon ended in sublamina b of the inner plexiform layer and provided major input to the AII amacrine cell. The axons of three types of cone bipolar cells also terminated in sublamina b and provided contacts to dendrites of on-beta and other ganglion cells. All three types, but especially the Cb1, received gap junction contacts from the AII amacrine cell. Axons of four types of cone bipolar cells terminated in sublamina a of the inner plexiform layer and contacted dendrites of off-beta and other ganglion cells. One of these cone bipolar cell types, CBa1, made reciprocal chemical contacts with the lobular appendage of the AII amacrine cell. These results show that the pattern of cone bipolar cell input to beta (X) and probably alpha (Y) ganglion cells is substantially more complex than had been suspected. At least two types of cone bipolar contribute to each type of ganglion cell where only a single type had been anticipated. In addition, many of the cone bipolar cell pathways in the inner plexiform layer are available to the rod system, since at least four types of cone bipolar receive electrical or chemical inputs from the AII amacrine cell. This may help to explain why, in a retina where rods far outnumber the cones, there should be so many types of cone bipolar cells.

[1]  B. Boycott,et al.  Organization of the primate retina: electron microscopy , 1966, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[2]  P. Sterling,et al.  Toward a functional architecture of the retina: serial reconstruction of adjacent ganglion cells. , 1980, Science.

[3]  H. Wässle,et al.  The mosaic of nerve cells in the mammalian retina , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[4]  B. Boycott,et al.  Morphology and mosaic of on- and off-beta cells in the cat retina and some functional considerations , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[5]  P Sterling,et al.  Interplexiform cell in cat retina: identification by uptake of gamma-[3H]aminobutyric acid and serial reconstruction. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[6]  R. Pourcho.  Uptake of [3H]glycine and [3H]GABA by amacrine cells in the cat retina , 1980, Brain Research.

[7]  M. Kidd.  Electron microscopy of the inner plexiform layer of the retina in the cat and the pigeon. , 1962, Journal of anatomy.

[8]  R. West.  Bipolar and horizontal cells of the gray squirrel retina: Golgi morphology and receptor connections , 1978, Vision Research.

[9]  Helga Kolb,et al.  Amacrine cells, bipolar cells and ganglion cells of the cat retina: A Golgi study , 1981, Vision Research.

[10]  H. J. Wyatt,et al.  Specific effects of neurotransmitter antagonists on ganglion cells in rabbit retina. , 1976, Science.

[11]  W. Pitts,et al.  Anatomy and Physiology of Vision in the Frog (Rana pipiens) , 1960, The Journal of general physiology.

[12]  H. Kolb,et al.  Intracellular staining reveals different levels of stratification for on- and off-center ganglion cells in cat retina. , 1978, Journal of neurophysiology.

[13]  B. Boycott,et al.  Topography of horizontal cells in the retina of the domestic cat , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[14]  R. Nelson,et al.  AII amacrine cells quicken time course of rod signals in the cat retina. , 1982, Journal of neurophysiology.

[15]  K Naka,et al.  Functional organization of catfish retina. , 1977, Journal of neurophysiology.

[16]  R W West,et al.  Synaptic connections of the interplexiform cell in the retina of the cat , 1977, Journal of neurocytology.

[17]  W. Levick,et al.  Properties of rarely encountered types of ganglion cells in the cat's retina and on overall classification , 1974, The Journal of physiology.

[18]  E. Raviola,et al.  Light and electron microscopic observations on the inner plexiform layer of the rabbit retina. , 1967, The American journal of anatomy.

[19]  I. Holmgren-Taylor.  Electron microscopical observations on the indoleamine‐accumulating neurons and their synaptic connections in the retina of the cat , 1982, The Journal of comparative neurology.

[20]  B. Boycott,et al.  The connections between bipolar cells and photoreceptors in the retina of the domestic cat , 1973, The Journal of comparative neurology.

[21]  Peter Sterling,et al.  A systematic approach to reconstructing microcircuitry by electron microscopy of serial sections , 1980, Brain Research Reviews.

[22]  Helga Kolb,et al.  Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina , 1983, Vision Research.

[23]  W. Stell,et al.  Retinal structure in the smooth dogfish, Mustelus canis: Light microscopy of bipolar cells , 1973, The Journal of comparative neurology.

[24]  R. Pourcho,et al.  Neuronal subpopulations in cat retina which accumulate the GABA agonist, (3H)muscimol: A combined Golgi and autoradiographic study , 1983, The Journal of comparative neurology.

[25]  R. Nelson,et al.  Cat cones have rod input: A comparison of the response properties of cones and horizontal cell bodies in the retina of the cat , 1977, The Journal of comparative neurology.

[26]  P. Sterling.  Microcircuitry of the cat retina. , 1983, Annual review of neuroscience.

[27]  Helga Kolb,et al.  Rod and Cone Pathways in the Inner Plexiform Layer of Cat Retina , 1974, Science.

[28]  N. Daw.  Neurophysiology of color vision. , 1973, Physiological reviews.

[29]  N. Daw,et al.  Opponent Color Cells in the Cat Lateral Geniculate Nucleus , 1970, Science.

[30]  E. V. Famiglietti,et al.  Structural basis for ON-and OFF-center responses in retinal ganglion cells. , 1976, Science.

[31]  P. Sterling.  IDENTIFIED NEURONS IN THE CAT RETINA , 1982 .

[32]  Helga Kolb,et al.  A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina , 1975, Brain Research.

[33]  A. Kaneko.  Physiological and morphological identification of horizontal, bipolar and amacrine cells in goldfish retina , 1970, The Journal of physiology.

[34]  E. V. Famiglietti,et al.  Functional architecture of cone bipolar cells in mammalian retina , 1981, Vision Research.

[35]  B. Boycott,et al.  Morphology and topography of on- and off-alpha cells in the cat retina , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[36]  N. Daw,et al.  Cat colour vision: one cone process or several? , 1969, The Journal of physiology.