Skip to main content
Log in

GABA-mediated inhibition of visual interneurons in the crayfish medulla

  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Summary

  1. 1.

    The actions of GABA on three classes of visual interneurons in crayfish, Procambarus clarkii, medulla externa are examined. The effect of GABA on the visual response is compared to GABA's action on agonist-elicited responses purported to mediate the visual response.

  2. 2.

    GABA produces a shunting type of inhibition in medullary amacrine cells which is associated with a small depolarization (Figs. 2, 3), a large increase in input conductance (Gn) and a reversal potential close to rest (Fig. 4). GABA is a potent antagonist to the depolarizing action of acetylcholine (ACh) (Fig. 5).

  3. 3.

    GABA depolarizes dimming fibers (Fig. 2), and the response is mediated by an increase in Gn (Fig. 6). GABA antagonizes the light-elicited IPSP and the hyperpolarizing action of ACh (Fig. 7).

  4. 4.

    Sustaining fibers (SF) do not appear to have GABA receptors but GABA inhibits the excitatory visual input pathway to the SFs (Fig. 8). Conversely, the GABA antagonist, bicuculline, potentiates the SF light response (Fig. 9).

  5. 5.

    GABA has at least three different modes of antagonist action in the medulla: i) Increased conductance and depolarization in dimming fibers and medullary amacrine neurons; ii) Decreased chloride conductance in tangential cells; and iii) An inhibitory action on the visual pathway which drives SFs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

DF :

dimming fiber

SF :

sustaining fiber

TAN1 :

tangential neuron

TM :

transmedullary neuron

References

  • Benson JA (1988) Bicuculline blocks the response to acetylcholine and nicotine but not to muscarine or GABA in isolated insect neuronal somata. Brain Res 458:65–71

    Article  CAS  PubMed  Google Scholar 

  • Blankenship JE, Wachtel H, Kandel ER (1971) Ionic mechanisms of excitatory, inhibitory and dual synaptic actions mediated by an identified interneuron in abdominal ganglion of Aplysia. J Neurophysiol 34:76–91

    Google Scholar 

  • Campos-Ortega JA (1974) Autoradiographic localization of gammaaminobutyric acid uptake in the lamina ganglionaris of Musca and Drosophila. Z Zellforsch 147:415–431

    Google Scholar 

  • Datum K-H, Weiler R, Zettler F (1986) Immunocytochemical demonstration of gamma-amino-butyric acid and glutamate decarboxylase in R7 photoreceptors and C2 centrifugal fibers in the blowfly visual system. J Comp Physiol A 159:241–249

    Google Scholar 

  • Elofsson R, Nässel DR, Myhrberg H (1977) A catecholaminergic neuron connecting the first two optic neuropiles (lamina ganglionaris and medulla externa) of the crayfish Pacifastacus leniusculus. Cell Tissue Res 182:287–297

    Google Scholar 

  • Franke Ch, Hatt H, Dudel J (1986) The inhibitory chloride channel activated by glutamate as well as gamma-amino-butyric acid (GABA). J Comp Physiol A 159:591–609

    Google Scholar 

  • Garcia H, Aréchiga H (1986) GABAergic input to crustacean neurosecretory cells. Neurosci Abstr 12:243

    Google Scholar 

  • Glantz R, Pfeiffer-Linn C (1990) Synaptic mechanisms of a dual channel contrast detection system in the crayfish optic lobe. In: Wiese K, Krenz W-D, Tautz J, Reichert H, Mulloney B (eds) Crustacean neurobiology. Birkhäuser, Berlin Zürich, pp 157–164

    Google Scholar 

  • Glantz RM, Wang-Bennett L, Waldrop B (1985) Presynaptic inhibition in the crayfish brain. Inhibition of a central synapse and synaptic events in presynaptic terminals. J Comp Physiol A 156:477–487

    Google Scholar 

  • Homberg K, Kingan TG, Hildebrand JG (1987) Immunocytochemistry of GABA in the brain and subesophageal ganglion of Manduca sexta. Cell Tissue Res 248:1–24

    Google Scholar 

  • Kehoe J (1972a) Ionic mechanism of a two-component cholinergic inhibition in Aplysia neurons. J Physiol (Lond) 225:85–114

    Google Scholar 

  • Kehoe J (1972b) Three acetylcholine receptors in Aplysia neurones. J Physiol 225:115–146

    Google Scholar 

  • Kennedy D, McVittie J, Calabrese R, Fricke RA, Craelius W, Chiapella P (1980) Inhibition of mechanosensory interneurons in the crayfish Procambarus clarkii. I: Presynaptic inhibition from giant fibers. J Neurophysiol 43:1495–1509

    Google Scholar 

  • Kirk MD (1982) The crayfish visual system: Intracellular studies and morphologies of identified neurons. Ph.D. Dissertation, Rice University, Houston Tx

    Google Scholar 

  • Kirk MD, Waldrop B, Glantz RM (1982) The crayfish sustaining fibers I: Morphological representation of visual receptive fields in the second optic neuropil. J Comp Physiol 146:175–179

    Google Scholar 

  • Marder EE (1976) Cholinergic motor neurones in the stomatogastric system of the lobster. J Physiol (Lond) 257:63–86

    Google Scholar 

  • Marder E, Paupardin-Tritsch D (1978) The pharmacological properties of some crustacean neuronal acetylcholine, gammaaminobutyric acid and L-glutamate responses. J Physiol 280: 213–236

    Google Scholar 

  • Maxwell GD, Hildebrand JG (1981) Anatomical and neurochemical consequences of deafferentation in the development of the visual system of the moth Manduca sexta. J Comp Neurol 195:667–680

    Google Scholar 

  • Meyer EP, Matute C, Streit P, Nässel DR (1986) Insect optic lobe neurons identifiable with monoclonal antibodies to GABA. Histochem 84:207–216

    Google Scholar 

  • Ochi R (1969) Ionic mechanisms of inhibitory postsynaptic potential of crayfish giant motor fiber. Pflügers Arch 311:131–143

    Google Scholar 

  • Pfeiffer C, Glantz RM (1989) Cholinergic synapses and the organization of contrast detection in the crayfish optic lobe. J Neurosce 9:1872–1882

    Google Scholar 

  • Pfeiffer-Linn CL, Glantz RM (1989a) Acetylcholine and GABA mediate opposing actions on neuronal chloride channels in crayfish. Science 245:1249–1251

    Google Scholar 

  • Pfeiffer-Linn CL, Glantz RM (1989b) Pharmacological evidence that glutamate is the excitatory neurotransmitter to an interneuron in the crayfish medulla. Soc Neurosci Abstr 15:26

    Google Scholar 

  • Pfeiffer-Linn C, Glantz RM (1990) A neuronal nicotinic acetylcholine receptor in crayfish neurons. Neurosci Lett (In press)

  • Stewart WW (1978) Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimide tracer. Cell 14:741–759

    Google Scholar 

  • Strausfeld NJ, Nässel DR (1981) Neuroarchitectures serving compound eyes of Crustacea and insects. In: Autrum H (ed) Vision in invertebrates (Handbook of sensory physiology, vol VII/6B). Springer, Berlin Heidelberg New York, pp 1–132

    Google Scholar 

  • Takeuchi A (1976) Studies of inhibitory effects of GABA in invertebrate nervous systems. In: Roberts E, Chase TN, Tower DB (eds) GABA in nervous system function. Raven Press, New York, pp 255–267

    Google Scholar 

  • Waldrop B, Glantz RM (1985a) Synaptic mechanisms of a tonic EPSP in crustacean visual interneurons: Analysis and simulation. J Neurophysiol 54:636–650

    Google Scholar 

  • Waldrop B, Glantz RM (1985b) Nonspiking local interneurons mediate surround inhibition in crayfish sustaining fibers. J Comp Physiol A 156:763–774

    Google Scholar 

  • Wang-Bennett LT, Glantz RM (1987a) The functional organization of the crayfish lamina ganglionaris. I. Nonspiking monopolar neurons. J Comp Physiol A 161:131–145

    Google Scholar 

  • Wang-Bennett LT, Glantz RM (1987b) The functional organization of the crayfish lamina ganglionaris. II. Large field spiking and nonspiking cells. J Comp Physiol A 161:147–160

    Google Scholar 

  • Wang-Bennett LT, Pfeiffer C, Arnold J, Glantz RM (1989) Acetylcholine in the crayfish optic lobe: Concentration profile and cellular localization. J Neurosci 9(6): 1864–1871

    Google Scholar 

  • Wiersma CAG, Yamaguchi T (1967) Integration of visual stimuli by the crayfish central nervous system. J Exp Biol 47: 409–431

    Google Scholar 

  • Yamaguchi T, Ohtsuka T (1973) Dual channeling mechanism of brightness and dimness information in the crayfish visual system. J Fac Sci Hokkaido Univ Ser VI Zool 19:15–30

    Google Scholar 

  • Yarowsky PJ, Carpenter DO (1978a) Comparison of similar ionic responses to gamma-aminobutyric acid and acetylcholine. J Neurophysiol 41:531–541

    CAS  PubMed  Google Scholar 

  • Yarowsky PJ, Carpenter DO (1978b) Receptors for gammaaminobutyric acid (GABA) on Aplysia neurons. Brain Res 144:75–94

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pfeiffer-Linn, C., Glantz, R.M. GABA-mediated inhibition of visual interneurons in the crayfish medulla. J Comp Physiol A 168, 373–381 (1991). https://doi.org/10.1007/BF00198356

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00198356

Key words

Navigation