Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-22T13:08:34.808Z Has data issue: false hasContentIssue false
  • English
  • Français

Cobalt ions inhibit negative feedback in the outer retina by blocking hemichannels on horizontal cells

Published online by Cambridge University Press:  01 July 2004

I. FAHRENFORT ,
T. SJOERDSMA ,
H. RIPPS  and
M. KAMERMANS
I. FAHRENFORT
Affiliation:
Research Unit Retinal Signal Processing, The Netherlands Ophthalmic Research Institute, Amsterdam, The Netherlands
T. SJOERDSMA
Affiliation:
Research Unit Retinal Signal Processing, The Netherlands Ophthalmic Research Institute, Amsterdam, The Netherlands
H. RIPPS
Affiliation:
Department of Ophthalmology and Visual Sciences, University of Illinois College of Medicine, Chicago
M. KAMERMANS
Affiliation:
Research Unit Retinal Signal Processing, The Netherlands Ophthalmic Research Institute, Amsterdam, The Netherlands
Get access Rights & Permissions [Opens in a new window]

Abstract

In goldfish, negative feedback from horizontal cells to cones shifts the activation function of the Ca2+ current of the cones to more negative potentials. This shift increases the amount of Ca2+ flowing into the cones, resulting in an increase in glutamate release. The increased glutamate release forms the basis of the feedback-mediated responses in second-order neurons, such as the surround-induced responses of bipolar cells and the spectral coding of horizontal cells. Low concentrations of Co2+ block these feedback-mediated responses in turtle retina. The mechanism by which this is accomplished is unknown. We studied the effects of Co2+ on the cone/horizontal network of goldfish retina and found that Co2+ greatly reduced the feedback-mediated responses in both cones and horizontal cells in a GABA-independent way. The reduction of the feedback-mediated responses is accompanied by a small shift of the Ca2+ current of the cones to positive potentials. We have previously shown that hemichannels on the tips of the horizontal cell dendrites are involved in the modulation of the Ca2+ current in cones. Both the absence of this Co2+-induced shift of the Ca2+ current in the absence of a hemichannel conductance and the sensitivity of Cx26 hemichannels to low concentrations of Co2+ are consistent with a role for hemichannels in negative feedback from horizontal cells to cones.

Keywords

Negative feedbackConesHorizontal cellsHemichannelsGABACo2+
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 4 , July 2004 , pp. 501 - 511
Copyright
2004 Cambridge University Press

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

Byzov, A.L., Golubtzov, K.V., & Trifonov, J.A. (1977). The model of mechanism of feedback between horizontal cells and photoreceptors in vertebrate retina. In Vertebrate photoreception, ed. Barlow, H.B. & Fatt, P., pp. 265–274. London-New York-San Francisco.
Byzov, A.L. & Shura-Bura, T.M. (1986). Electrical feedback mechanism in the processing of signals in the outer plexiform layer of the retina. Vision Research 26, 33–44.CrossRefGoogle Scholar
Dowling, J.E. (1987). The Retina. An Approachable Part of the Brain, 1st edition. Cambridge: Belknap Press.
Fahrenfort, I., Habets, R.L., Spekreijse, H., & Kamermans, M. (1999). Intrinsic cone adaptation modulates feedback efficiency from horizontal cells to cones. Journal of General Physiology 114, 511–524.CrossRefGoogle Scholar
Hanitzsch, R. & Kuppers, L. (2001). The influence of HEPES on light responses of rabbit horizontal cells. Vision Research 41, 2165–2172.CrossRefGoogle Scholar
Hille, B. (1992). Ionic Channels of Excitable Membranes. Sunderland, Massachusetts: Sinauer Associates Inc..
Hirasawa, H. & Kaneko, A. (2003). pH changes in the invaginating synaptic cleft mediate feedback from horizontal cells to cone photoreceptors by modulating Ca2+ channels. Journal of General Physiology 122, 657–671.CrossRefGoogle Scholar
Kamermans, M. & Spekreijse, H. (1999). The feedback pathway from horizontal cells to cones in the goldfish retina. Vision Research 39, 2449–2468.CrossRefGoogle Scholar
Kamermans, M., Van Dijk, B.W., & Spekreijse, H. (1991). Color opponency in cone-driven horizontal cells in carp retina. Aspecific pathways between cones and horizontal cells. Journal of General Physiology 97, 819–843.Google Scholar
Kamermans, M., Kraaij, D.A., & Spekreijse, H. (1998). The cone/horizontal cell system: A possible site for color-constancy. Visual Neuroscience 15, 787–797.Google Scholar
Kamermans, M., Kraaij, D.A., & Spekreijse, H. (2001). The dynamics characteristics of the feedback signal from horizontal cells to cones in the goldfish retina. Journal of Physiology 534.2, 489–500.CrossRefGoogle Scholar
Kaneko, A. & Tachibana, M. (1986). Effects of gamma-aminobutyric acid on isolated cone photoreceptors of the turtle retina. Journal of Physiology 373, 443–461.CrossRefGoogle Scholar
Kaneko, A. & Hirasawa, H. (2003). Neural circuit contributing to the formation of the receptive receptive surround. In The Neural Basis of Early Vision, ed. Kaneko, A., pp. 42–43. New York: Springer.CrossRef
Kraaij, D.A., Spekreijse, H., & Kamermans, M. (2000). The open- and closed-loop gain—characteristics of the cone/horizontal cell synapse in goldfish retina. Journal of Neurophysiology 84, 1256–1265.Google Scholar
Kreitzer, M.A., Andersen, K.A., & Malchow, R.P. (2003). Glutamate modulation of GABA transport in retinal horizontal cells of the skate. Journal of Physiology 546, 717–731.CrossRefGoogle Scholar
Mangel, S.C., Ariel, M., & Dowling, J.E. (1985). Effects of acidic amino acid antagonists upon the spectral properties of carp horizontal cells: Circuitry of the outer retina. Journal of Neuroscience 5, 2839–2850.Google Scholar
Marc, R.E., Stell, W.K., Bok, D., & Lam, D.M.K. (1978). GABA-ergic pathways in the goldfish retina. Journal of Comparative Neurology 182, 221–246.CrossRefGoogle Scholar
Perlman, I. & Normann, R.A. (1990). The effect of GABA and related drugs on horizontal cells in the isolated turtle retina. Visual Neuroscience 5, 469–477.CrossRefGoogle Scholar
Piccolino, M., Pignatelli, A., & Rakotobe, L.A. (1999). Calcium-independent release of neurotransmitter in the retina: A copernican viewpoint change. Progress in Retinal and Eye Research 18, 1–38.CrossRefGoogle Scholar
Ripps, H., Qian, H., & Zakevicius, J. (2002). Pharmacological enhancement of hemi-gap-junctional currents in Xenopus oocytes. Journal of Neuroscience Methods 121, 81–92.CrossRefGoogle Scholar
Schmidt, K.F. (1999). Divalent cations modulate glutamate receptors in retinal horizontal cells of the perch (Perca fluviatilis). Neuroscience Letters 262, 109–112.CrossRefGoogle Scholar
Schwartz, E.A. (1987). Depolarization without calcium can release gamma-aminobutyic acid from a retinal neuron. Science 238, 350–355.CrossRefGoogle Scholar
Stell, W.K. & Lightfoot, D.O. (1975). Color-specific interconnections of cones and horizontal cells in the retina of the goldfish. Journal of Comparative Neurology 159, 473–502.CrossRefGoogle Scholar
Takahashi, K.-I., Miyoshi, S.-I., Kaneko, A., & Copenhagen, D.R. (1995). Actions of nipecotic acid and SKF89976A on GABA transporter in cone-driven horizontal cells dissociated from the catfish retina. Japanese Journal of Physiology 45, 457–473.CrossRefGoogle Scholar
Thoreson, W.B. & Burkhardt, D.A. (1990). Effects of synaptic blocking agents on the depolarizing responses of turtle cones evoked by surround illumination. Visual Neuroscience 5, 571–583.CrossRefGoogle Scholar
Verweij, J., Kamermans, M., & Spekreijse, H. (1996). Horizontal cells feed back to cones by shifting the cone calcium-current activation range. Vision Research 36, 3943–3953.CrossRefGoogle Scholar
Verweij, J., Kamermans, M., Negishi, K., & Spekreijse, H. (1998). GABA-sensitivity of spectrally classified horizontal cells in the goldfish retina. Visual Neuroscience 15, 77–86.Google Scholar
Verweij, J., Hornstein, E.P., & Schnapf, J.L. (2003). Surround antagonism in macaque cone photoreceptors. Journal of Neuroscience 23, 10249–10257.Google Scholar
Vigh, J. & Witkovsky, P. (1999). Sub-millimolar cobalt selectively inhibits the receptive field surround of retinal neurons. Visual Neuroscience 16, 159–168.CrossRefGoogle Scholar
Weiler, R. & Wagner, H.-J. (1984). Light-dependent change of cone-horizontal cell interactions in carp retina. Brain Research 298, 1–9.Google Scholar
Witkovsky, P., Gabriel, R., Krizaj, D., & Akopian, A. (1995). Feedback from luminosity horizontal cells mediates depolarizing responses of chromaticity horizontal cells in the Xenopus retina. Proceedings of the National Academy of Sciences of the U.S.A. 92, 3556–3560.CrossRefGoogle Scholar
Wu, S.M. (1994). Synaptic transmission in the outer retina. Annual Reviews of Physiology 56, 141–168.CrossRefGoogle Scholar