Presynaptic inhibition by GABA is mediated via two distinct GABA receptors with novel pharmacology

Matthews, Gary; Ayoub, George; Heidelberger, Ruth

doi:10.1523/jneurosci.14-03-01079.1994

Cited by 110 publications

(88 citation statements)

References 39 publications

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“…4 B). This prediction is in good agreement with a previous finding that GABA receptors can significantly inhibit potassium-induced depolarizations and Ca 2ϩ influx into isolated goldfish bipolar cell terminals (Matthews et al, 1994).…”

Section: Gat-1 Transporters Limit Reciprocal Activation Of Gaba C Recsupporting

confidence: 93%

GABA Transporters Regulate a Standing GABA_CReceptor-Mediated Current at a Retinal Presynaptic Terminal

Hull

Gersdorff

2006

J. Neurosci.

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At the axon terminal of goldfish retinal bipolar cells, GABA C receptors have been shown to mediate inhibitory reciprocal synaptic currents. Here, we demonstrate a novel standing GABAergic current mediated exclusively by GABA C receptors. Selective inhibition of GAT-1 GABA transporters on amacrine cells increases this tonic current and reveals a specific functional coupling between GAT-1 transporters and GABA C receptors. We propose that this GABA C receptor-mediated standing current serves to regulate synaptic gain by shunting depolarizing potentials that can produce Ca

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Section: Gat-1 Transporters Limit Reciprocal Activation Of Gaba C Recsupporting

confidence: 93%

GABA Transporters Regulate a Standing GABA_CReceptor-Mediated Current at a Retinal Presynaptic Terminal

Hull

Gersdorff

2006

J. Neurosci.

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“…Though picrotoxin was an effective antagonist of GABA responses in isolated cells, a GABA response component sometimes remained (see Figure 6C), indicating an insensitive component could also be present on the dendrites. Though picrotoxin-insensitive GABA C receptors have been identified in rat bipolar cells (Feigenspan et al, 1993;Feigenspan & Bormann, 1994), this finding is in contrast to reports from other teleost retinas (Tachibana & Kaneko, 1987;Qian & Dowling, 1993;Matthews et al, 1994;Qian & Dowling, 1994Han et al, 1997).…”

Section: Gaba Receptors On Zebrafish Bipolar Cells Have Unique Antagocontrasting

confidence: 99%

Electrophysiological evidence of GABA_A and GABA_C receptors on zebrafish retinal bipolar cells

2008

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To refine inhibitory circuitry models for ON and OFF pathways in zebrafish retina, GABAergic properties of zebrafish bipolar cells were studied with two techniques: whole cell patch responses to GABA puffs in retinal slice, and voltage probe responses in isolated cells. Retinal slices documented predominantly axon terminal responses; isolated cells revealed mainly soma-dendritic responses. In the slice, GABA elicited a conductance increase, GABA responses were more robust at axon terminals than dendrites, and E rev varied with [Cl − ] in . Axon terminals of ON-and OFFtype cells were similarly sensitive to GABA (30-40pA peak current); axotomized cells were unresponsive. Bicuculline-sensitive, picrotoxin-sensitive, and picrotoxin-insensitive components were identified. Muscimol was as effective as GABA; baclofen was ineffective. Isolated bipolar cells were either intact or axotomized. Even in cells without an axon, GABA or muscimol (but not baclofen) hyperpolarized dendritic and somatic regions, suggesting significant distal expression. Median fluorescence change for GABA was −0.22 log units (~−16mV); median half-amplitude dose was 0.4μM. Reduced [Cl − ] out blocked GABA responses. GABA hyperpolarized isolated ONbipolar cells, OFF-cells were either unresponsive or depolarized. Hyperpolarizing GABA responses in isolated cells were bicuculline and TPMPA insensitive, but blocked or partially blocked by picrotoxin or zinc. In summary, axon terminals contain bicuculline-sensitive GABA A

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“…Our results imply that in Drosophila this is mediated by both GABA A and GABA B receptors. This arrangement is unusual but not unique; for example, there are several instances of GABA A and GABA B inhibition at the same presynaptic site in other neural circuits [36][37][38][39] . Ionotropic and metabotropic receptors act with different kinetics, and so this arrangement might ensure that inhibition spans a broad time window.…”

Section: Discussionmentioning

confidence: 99%

Lateral presynaptic inhibition mediates gain control in an olfactory circuit

Olsen

Wilson

2008

Nature

482

555

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SUMMARYOlfactory signals are transduced by a large family of odorant receptor proteins, each of which corresponds to a unique glomerulus in the first olfactory relay of the brain. Cross-talk between glomeruli has been proposed to be important in olfactory processing, but it is not clear how these interactions shape the odor responses of second-order neurons. In the Drosophila antennal lobe (a region analogous to the vertebrate olfactory bulb), we selectively remove most inter-glomerular input to identified second-order olfactory neurons. We find this broadens the odor tuning of these neurons, implying that inter-glomerular inhibition dominates over inter-glomerular excitation. The strength of this inhibitory signal scales with total feedforward input to the entire antennal lobe, and has similar tuning in different glomeruli. A substantial portion of this inter-glomerular inhibition acts at a presynaptic locus, and our results imply this is mediated by both GABA A and GABA B receptors on the same nerve terminal.A sensory stimulus generally triggers activity in multiple neural processing channels, each of which carries information about some feature of that stimulus. The concept of a processing channel has a particularly clear anatomical basis in the first relay of the olfactory system, which is typically divided into glomerular compartments. Each glomerulus receives input from many first-order olfactory receptor neurons (ORNs), all of which express the same odorant receptor. Each second-order neuron receives direct ORN input from a single glomerulus, and thus all the first-and second-order neurons corresponding to a glomerulus constitute a discrete processing channel. An odorant typically triggers activity in multiple glomeruli, and local interneurons that interconnect glomeruli provide a substrate for cross-talk between channels.The Drosophila antennal lobe is a favored model for investigating olfactory processing because it contains only ~50 glomeruli 1 , each of which corresponds to an identified type of ORN and an identified type of postsynaptic projection neuron (PN) 2-5. Several recent studies of the Drosophila antennal lobe have produced divergent views of the relative importance of interglomerular connections. One model proposes that PN odor responses are almost completely determined by feedforward excitation6 , 7. This model ascribes little importance to cross-talk between glomerular processing channels. An alternative model proposes that inter-glomerular connections make an important contribution to shaping PN odor responses8 -12 . However, thisCorrespondence and requests for materials should be addressed to R.I.W. (rachel_wilson@hms.harvard.edu). Full Methods are available in the online version of the paper at www.nature.com/nature.Supplementary Information is linked to the online version of the paper at www.nature.com/nature. A figure summarizing the main result of this paper is available in Supplementary Information. . This could reflect a purely intra-glomerular nonlinear process, such as short-term...

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Presynaptic inhibition by GABA is mediated via two distinct GABA receptors with novel pharmacology

Cited by 110 publications

References 39 publications

GABA Transporters Regulate a Standing GABA_CReceptor-Mediated Current at a Retinal Presynaptic Terminal

GABA Transporters Regulate a Standing GABA_CReceptor-Mediated Current at a Retinal Presynaptic Terminal

Electrophysiological evidence of GABA_A and GABA_C receptors on zebrafish retinal bipolar cells

Lateral presynaptic inhibition mediates gain control in an olfactory circuit

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Presynaptic inhibition by GABA is mediated via two distinct GABA receptors with novel pharmacology

Cited by 110 publications

References 39 publications

GABA Transporters Regulate a Standing GABACReceptor-Mediated Current at a Retinal Presynaptic Terminal

GABA Transporters Regulate a Standing GABACReceptor-Mediated Current at a Retinal Presynaptic Terminal

Electrophysiological evidence of GABAA and GABAC receptors on zebrafish retinal bipolar cells

Lateral presynaptic inhibition mediates gain control in an olfactory circuit

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Product

Resources

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GABA Transporters Regulate a Standing GABA_CReceptor-Mediated Current at a Retinal Presynaptic Terminal

GABA Transporters Regulate a Standing GABA_CReceptor-Mediated Current at a Retinal Presynaptic Terminal

Electrophysiological evidence of GABA_A and GABA_C receptors on zebrafish retinal bipolar cells