Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-25T14:57:36.613Z Has data issue: false hasContentIssue false
  • English
  • Français

Physiology of the A1 amacrine: A spiking, axon-bearing interneuron of the macaque monkey retina

Published online by Cambridge University Press:  02 June 2009

Donna K. Stafford  and
Dennis M. Dacey
Donna K. Stafford
Affiliation:
Department of Biological Structure, University of Washington, Seattle
Dennis M. Dacey
Affiliation:
Department of Biological Structure, University of Washington, Seattle
Get access Rights & Permissions [Opens in a new window]

Abstract

We characterized the light response, morphology, and receptive-field structure of a distinctive amacrine cell type (Dacey, 1989), termed here the Al amacrine, by applying intracellular recording and staining methods to the macaque monkey retina in vitro. A1 cells show two morphologically distinct components: a highly branched and spiny dendritic tree, and a more sparsely branched axon-like tree that arises from one or more hillock-like structures near the soma and extends for several millimeters beyond the dendritic tree. Intracellular injection of Neurobiotin reveals an extensive and complex pattern of tracer coupling to neighboring A1 amacrine cells, to two other amacrine cell types, and to a single ganglion cell type. The A1 amacrine is an ON-OFF cell, showing a large (10–20 mV) transient depolarization at both onset and offset of a photopic, luminance modulated stimulus. A burst of fast, large-amplitude (Σ60 mV) action potentials is associated with the depolarizations at both the ON and OFF phase of the response. No evidence was found for an inhibitory receptive-field surround. The spatial extent of the ON-OFF response was mapped by measuring the strength of the spike discharge and/or the amplitude of the depolarizing slow potential as a function of the position of a bar or spot of light within the receptive field. Receptive fields derived from the slow potential and associated spike discharge corresponded in size and shape. Thus, the amplitude of the slow potential above spike threshold was well encoded as spike frequency. The diameter of the receptive field determined from the spike discharge was Σ10% larger than the spiny dendritic field. The correspondence in size between the spiking receptive field and the spiny dendritic tree suggests that light driven signals are conducted to the soma from the dendritic tree but not from the axon-like arbor. The function of the axon-like component is unknown but we speculate that it serves a classical output function, transmitting spikes distally from initiation sites near the soma.

Keywords

Macaque monkey retinaAmacrine cellsSpikesTracer coupling
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 3 , May 1997 , pp. 507 - 522
Copyright
Copyright © Cambridge University Press 1997

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ammermüller, J. & Weiler, R. (1989). Correlation between electrophysiological responses and morphological classes of turtle retinal amacrine cells. In Neurobiology of the Inner Retina—NATO ASI Series, Vol. H31, ed. Weiler, R. & Osborne, N.N., pp. 117–132. Berlin-Heidelberg: Springer-Verlag.Google Scholar
Bloomfield, S.A. (1991). Two types of orientation-sensitive responses of amacrine cells in the mammalian retina. Nature 350, 347–350.Google Scholar
Bloomfield, S.A. (1992). Relationship between receptive and dendritic field size of amacrine cells in the rabbit retina. Journal of Neurophysiology 68, 711–725.Google Scholar
Bloomfield, S.A. (1996). Effect of spike blockade on the receptive-field size of amacrine and ganglion cells in the rabbit retina. Journal of Neurophysiology 75, 1878–1893.Google Scholar
Catsicas, S., Catsicas, M. & Clarke, P.G.H. (1987). Long-distance intraretinal connections in birds. Nature 326, 186–187.CrossRefGoogle ScholarPubMed
Cook, P.B. & Werblin, F.S. (1994). Spike initiation and propagation in wide field transient amacrine cells of the salamander retina. Journal of Neuroscience 14, 3852–3861.CrossRefGoogle ScholarPubMed
Dacey, D.M. (1988). Dopamine-accumulating retinal neurons revealed by in vitro fluorescence display a unique morphology. Science 240, 1196–1198.Google Scholar
Dacey, D.M. (1989). Axon-bearing amacrine cells of the macaque monkey retina. Journal of Comparative Neurology 284, 275–293.Google Scholar
Dacey, D.M. (1990 a). The dopaminergic amacrine cell. Journal of Comparative Neurology 31, 461–489.Google Scholar
Dacey, D.M. (1990 b). Distinct cell types in living macaque retina display an unexpected granular fluorescence. Society for Neuroscience Abstracts 16, 466.Google Scholar
Dacey, D.M. (1990 c). The dopaminergic amacrine cells of the cat retina. Investigative Ophthalmology and Visual Science (Suppl.) 31, 535.Google Scholar
Dacey, D.M. (1996). Circuitry for color coding in the primate retina. Proceedings of the National Academy of Sciences of the U.S.A. 93, 582–588.Google Scholar
Dacey, D.M. & Brace, S. (1992). A coupled network for parasol but not midget ganglion cells in the primate retina. Visual Neuroscience 9, 279–290.Google Scholar
Dacey, D.M. (1993). The mosaic of midget ganglion cells in the human retina. Journal of Neuroscience 13, 5334–5355.Google Scholar
Dacey, D.M. & Lee, B.B. (1994). The “blue-on” opponent pathway in primate retina originates from a distinct bistratified ganglion cell type. Nature 367, 731–735.Google Scholar
Dacey, D.M., Lee, B.B., Stafford, D.K., Pokorny, J. & Smith, V.C. (1996). Horizontal cells of the primate retina: Cone specificity without spectral opponency. Science 271, 656–659.Google Scholar
Djamgoz, M.B.A., Downing, J.E.G., Kirsch, M., Prince, D.J. & Wagner, H.-J. (1988). Plasticity of cone horizontal cell functioning in cyprinid fish retina: Effects of background illumination of moderate intensity. Journal of Neurocytology 17, 701–710.Google Scholar
Djamgoz, M.B.A., Downing, J.E.G. & Wagner, H.-J. (1989). Amacrine cells in the retina of a cyprinid fish: Functional characterization and intracellular labelling with horseradish peroxidase. Cell and Tissue Research 256, 607–622.Google Scholar
Djamgoz, M.B.A. & Vallerga, S. (1989). Structure-function correlation: Amacrine cells of fish and amphibian retinae. In Neurobiology of the Inner Retina—NATO AS1 Series, Vol. H31, ed. Weiler, R. & Osborne, N.N., pp. 195–208. Berlin Heidelberg: Springer-Verlag.Google Scholar
Famiglietti, E.V. (1990). A new type of wide-field horizontal cell, presumably linked to blue cones, in rabbit retina. Brain Research 535, 174–179.Google Scholar
Famiglietti, E.V. (1992 a). Polyaxonal amacrine cells of rabbit retina: PA2, PA3, and PA4 cells. Light and electron microscopic studies with a functional interpretation. Journal of Comparative Neurology 316, 422–446.Google Scholar
Famiglietti, E.V. (1992 b). Polyaxonal amacrine cells of rabbit retina: Morphology and stratification of PA1 cells. Journal of Comparative Neurology 316, 391–405.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. Jr (1983). ‘Starburst’ amacrine cells and cholinergic neurons: Mirror-symmetric on and off amacrine cells of rabbit retina. Brain Research 261, 138–144.Google Scholar
Freed, M.A., Pflug, R., Kolb, H., Nelson, R. (1996). ON-OFF amacrine cells in cat retina. Journal of Comparative Neurology 364, 556–566.Google Scholar
Heimer, C.V. & Taylor, C.E.D. (1974). Improved mountant for immunofluorescent preparations. Journal of Clinical Pathology 27, 254–256.Google Scholar
Jensen, R.J. (1995). Receptive-field properties of displaced starburst amacrine cells change following axotomy-induced degeneration of ganglion cells. Visual Neuroscience 12, 177–184.Google Scholar
Kaneko, A. (1970). Physiological and morphological identification of horizontal bipolar and amacrine cells in goldfish retina. Journal of Physiology 207, 623–633.Google Scholar
Lee, B.B., Pokorny, J., Smith, V.C., Martin, P.R. & Valberg, A. (1990). Luminance and chromatic modulation sensitivity of macaque ganglion cells and human observers. Journal of Optical Society of America A 7, 2223–2236.Google Scholar
Maguire, G., Lukasiewicz, P. & Werblin, F. (1989). Amacrine cell interactions underlying the response to change in the tiger salamander retina. Journal of Neuroscience 9, 726–735.Google Scholar
Matsumoto, N. & Naka, K.I. (1972). Identification of intracellular responses in the frog retina. Brain Research 42, 59–71.Google Scholar
Miller, R.F. & Dacheux, R. (1976). Dendritic and somatic spikes in mudpuppy amacrine cells: Identification and TTX sensitivity. Brain Research 104, 157–162.Google Scholar
Miller, R.F. & Bloomfield, S.A. (1983). Electroanatomy of a unique amacrine cell in the rabbit retina. Proceedings of the National Academy of Sciences of the U.S.A. 80, 3069–3073.Google Scholar
Peters, B.N. & Masland, R.H. (1996). Responses to light of starburst amacrine cells. Journal of Neurophysiology 75, 469–480.Google Scholar
Rodieck, R.W. (1988). The primate retina. In Comparative Primate Biology, Vol. 4: Neurosciences, ed. Steklis, H.D., pp. 203–278. New York: Alan R. Liss, Inc.Google Scholar
Rodieck, R.W. & Marshak, D.W. (1992). Spatial density and distribution of choline acetyltransferase immunoreactive cells in human, macaque, and baboon retinas. Journal of Comparative Neurology 321, 46–64.Google Scholar
Sagar, S.M. (1987). Somatostatin-like immunoreactive material in the rabbit retina: Immunohistochemical staining using monoclonal antibodies. Journal of Comparative Neurology 266, 291–299.Google Scholar
Swanson, W.H., Ueno, T., Smith, V.C. & Pokorny, J. (1987). Temporal modulation sensitivity and pulse-detection thresholds for chromatic and luminance perturbations. Journal of the Optical Society of America 4, 1992–2005.Google Scholar
Tauchi, M. & Masland, R.H. (1984). The shape and arrangement of the cholinergic neurons in the rabbit retina. Proceedings of the Royal Society B (London) 223, 101–119.Google Scholar
Taylor, W.R. (1996). Response properties of long-range axon-bearing amacrine cells in the dark-adapted rabbit retina. Visual Neuroscience 13, 599–604.CrossRefGoogle ScholarPubMed
Taylor, W.R. & Wässle, H. (1995). Receptive field properties of starburst cholinergic amacrine cells in the rabbit retina. European Journal of Neuroscience 7, 2308–2321.CrossRefGoogle ScholarPubMed
Teranishi, T., Negishi, K. & Kato, S. (1987). Functional and morphological correlates of amacrine cells in carp retina. Neuroscience 20, 935–950.CrossRefGoogle ScholarPubMed
Vaney, D.I., Peichl, L. & Boycott, B.B. (1988). Neurofibrillar long-range amacrine cells in the mammalian retinae. Proceedings of the Royal Society B (London) 235, 203–219.Google Scholar
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. Progress in Retinal Research 9, 49–100.Google Scholar
Vaney, D.I. (1992). Photochromic intensification of diaminobenzidine reaction product in the presence of tetrazolium salts: applications for intracellular labelling and immunohistochemistry. Journal of Neuroscience Methods 44, 217–223.Google Scholar
Vaney, D.I. (1994). Patterns of neuronal coupling in the retina. In Progress in Retinal and Eye Research, ed. Osborne, N.N. & Chader, G.J., pp. 301–355. Great Britain: Pergamon Press Ltd.Google Scholar
Wässle, H. & Boycott, B.B. (1991). Functional architecture of the mammalian retina. Physiological Reviews 71, 447–480.Google Scholar
Wässle, H., Boycott, B.B. & Röhrenbeck, J. (1989). Horizontal cells in the monkey retina: Cone connections and dendritic network. European Journal of Neuroscience 1, 421–435.Google Scholar
Wässle, H., Grünert, U., Chun, M.H. & Boycott, B.B. (1995). The rod pathway of the macaque monkey retina: Identification of AII-amacrine cells with antibodies against calretinin. Journal of Comparative Neurology 361, 537–551.Google Scholar
Wässle, H. & Riemann, H.J. (1978). The mosaic of nerve cells in the mammalian retina. Proceedings of the Royal Society B (London) 200, 441–461.Google ScholarPubMed
Werblin, F. & Dowling, J.E. (1969). Organization of the retina of the mudpuppy, Necturus maculosus II Intracellular recording. Journal of Neurophysiology 32, 339–355.Google Scholar
Werblin, F.S. (1972). Lateral interactions at inner plexiform layer of vertebrate retina: Antagonistic response to change. Science 175, 1008–1010.Google Scholar
Werblin, F.S. & Copenhagen, D.R. (1974). Control of retinal sensitivity III. Lateral interactions at the inner plexiform layer. Journal of General Physiology 63, 88–110.Google Scholar
White, C.A., Chalupa, L.M., Johnson, D. & Brecha, N.C. (1990). Somatostatin-immunoreactive cells in the adult cat retina. Journal of Comparative Neurology 293, 134–150.Google Scholar