Evidence for GABAB-mediated inhibition of transmission from the olfactory nerve to mitral cells in the rat olfactory bulb

Nickell, William T.; Behbehani, Michael M.; Shipley, Michael T.

doi:10.1016/0361-9230(94)90091-4

Cited by 66 publications

(82 citation statements)

References 21 publications

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“…Previous studies in other species have shown that GABA can inhibit release from ORN axon terminals [15][16][17][18][19][20][21] . Our results imply that in Drosophila this is mediated by both GABA A and GABA B receptors.…”

Section: Discussionmentioning

confidence: 92%

“…We reasoned that some lateral inhibition might target ORN axon terminals; if so, this would only be observed when the direct ORN inputs to a PN are active. GABAergic inhibition at ORN axon terminals has been described previously in the olfactory bulb [15][16][17][18][19][20][21] , and synapses from GABAergic interneurons onto ORN axon terminals have been found in an insect antennal lobe 22 .To test the idea that some lateral inhibition is presynaptic, we asked how lateral input to glomerulus VM7 depends on the activity of VM7 ORNs. Each VM7 ORN fires spontaneously at ~10 spikes/s, and consequently these PNs are bombarded by spontaneous spike-driven EPSPs ( Supplementary Fig.…”

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confidence: 95%

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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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Section: Discussionmentioning

confidence: 92%

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confidence: 95%

Lateral presynaptic inhibition mediates gain control in an olfactory circuit

Olsen

Wilson

2008

Nature

482

555

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“…In the mammalian olfactory bulb (OB), GABA released from periglomerular interneurons suppresses ORN input via GABA B receptors expressed on the ORN terminal (Nickell et al, 1994;Bonino et al, 1999;Kratskin et al, 2006), and, in OB slice preparations, this transmitter pathway appears to be the major mediator of stimulus-evoked presynaptic inhibition (Aroniadou-Anderjaska et al, 2000;McGann et al, 2005;Wachowiak et al, 2005). In vivo, GABA B -mediated inhibition modulates the strength of odorant-evoked inputs to the OB , but many of the functional determinants of this inhibition remain unclear.…”

Section: Introductionmentioning

confidence: 99%

“…Likewise, previous studies in OB slices asking whether tonic GABA B inputs in vivo has not been addressed. Other predictions of the functional role of presynaptic inhibition in odor coding include rapid adaptive gain control, modulating the strength of sensory input as a function of sniffing frequency, and modulating input sensitivity as a function of behavioral state (Nickell et al, 1994;McGann et al, 2005;Wachowiak and Shipley, 2006). These predictions derive from experiments in OB slice preparations but have not been tested in vivo.…”

Section: Introductionmentioning

confidence: 99%

In Vivo Modulation of Sensory Input to the Olfactory Bulb by Tonic and Activity-Dependent Presynaptic Inhibition of Receptor Neurons

Pírez¹,

Wachowiak²

2008

Journal of Neuroscience

115

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The first reorganization of odor representations in the nervous system occurs at the synapse between olfactory receptor neurons and second-order neurons in olfactory bulb glomeruli. Signal transmission at this synapse is modulated presynaptically by several mechanisms, a major one being mediated by GABA B receptors, which suppress presynaptic calcium influx and subsequent transmitter release from the receptor neuron terminal. Here, we imaged stimulus-evoked calcium influx into the receptor neuron terminal in anesthetized mice and used odorant and electrical stimulation combined with in vivo pharmacology to characterize the functional determinants of GABA B -mediated presynaptic inhibition and to test hypotheses on the role of this inhibition in olfactory processing. As expected from previous studies, blocking presynaptic GABA B receptors in vivo increased odorant-evoked presynaptic calcium signals, confirming that GABA B -mediated inhibition modulates the strength of receptor inputs. Surprisingly, we found that the strength of this inhibition was affected little by the nature of the input, being independent of the spatial distribution of activated glomeruli, independent of the sniff frequency used to sample the odorant, and similar for weak and strong odorant-evoked inputs. Instead, we found that tonic inhibition was a major determinant of receptor input strength; this tonic inhibition in turn was dependent on glutamatergic transmission from second-order neurons in the glomerular layer. Thus, rather than adaptively shaping odor representations in an activity-dependent manner, a primary role of presynaptic inhibition in vivo may be to modulate the magnitude of sensory input to the brain as a function of behavioral state.

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“…In the rat main olfactory bulb, the glomeruli have the highest concentration of GABA B -Rs as determined by radioligand binding (Bowery et al 1987;Chu et al 1990) and by immunohistochemical localization of GABA B -R subunits (Bonino et al 1999;MargetaMitrovic et al 1999). There is now strong evidence for GABA B -R-mediated presynaptic inhibition of glutamate release from olfactory nerve terminals (Aroniadou-Anderjaska et al 2000;Keller et al 1998;Murphy et al 2005;Nickell et al 1994;Palouzier-Paulignan et al 2002;Vucinic et al 2006;Wachowiak and Cohen 1999;Wachowiak et al 2005). However, it is unknown whether GABA B -Rs are located postsynaptically on juxtaglomerular (JG) cells and whether they can modulate the bursting pattern of external tufted (ET) cells.…”

Section: Introductionmentioning

confidence: 99%

Activation of Postsynaptic GABA_BReceptors Modulates the Bursting Pattern and Synaptic Activity of Olfactory Bulb Juxtaglomerular Neurons

Karpuk

Hayar²

2008

Journal of Neurophysiology

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Olfactory bulb glomeruli are formed by a network of three major types of neurons collectively called juxtaglomerular (JG) cells, which include external tufted (ET), periglomerular (PG), and short axon (SA) cells. There is solid evidence that γ-aminobutyric acid (GABA) released from PG neurons presynaptically inhibits glutamate release from olfactory nerve terminals via activation of GABA B receptors (GABA B -Rs). However, it is still unclear whether ET cells have GABA B -Rs. We have investigated whether ET cells have functional postsynaptic GABA B -Rs using extracellular and whole cell recordings in olfactory bulb slices. In the presence of fast synaptic blockers (CNQX, APV, and gabazine), the GABA B -R agonist baclofen either completely inhibited the bursting or reduced the bursting frequency and increased the burst duration and the number of spikes/burst in ET cells. In the presence of fast synaptic blockers and tetrodotoxin, baclofen induced an outward current in ET cells, suggesting a direct postsynaptic effect. Baclofen reduced the frequency and amplitude of spontaneous EPSCs in PG and SA cells. In the presence of sodium and potassium channel blockers, baclofen reduced the frequency of miniature EPSCs, which were inhibited by the calcium channel blocker cadmium. All baclofen effects were reversed by application of the GABA B -R antagonist CGP55845. We suggest that activation of GABA B -Rs directly inhibits ET cell bursting and decreases excitatory dendrodendritic transmission from ET to PG and SA cells. Thus the postsynaptic GABA B -Rs on ET cells may play an important role in shaping the activation pattern of the glomeruli during olfactory coding.

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Evidence for GABAB-mediated inhibition of transmission from the olfactory nerve to mitral cells in the rat olfactory bulb

Cited by 66 publications

References 21 publications

Lateral presynaptic inhibition mediates gain control in an olfactory circuit

Lateral presynaptic inhibition mediates gain control in an olfactory circuit

In Vivo Modulation of Sensory Input to the Olfactory Bulb by Tonic and Activity-Dependent Presynaptic Inhibition of Receptor Neurons

Activation of Postsynaptic GABA_BReceptors Modulates the Bursting Pattern and Synaptic Activity of Olfactory Bulb Juxtaglomerular Neurons

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Evidence for GABAB-mediated inhibition of transmission from the olfactory nerve to mitral cells in the rat olfactory bulb

Cited by 66 publications

References 21 publications

Lateral presynaptic inhibition mediates gain control in an olfactory circuit

Lateral presynaptic inhibition mediates gain control in an olfactory circuit

In Vivo Modulation of Sensory Input to the Olfactory Bulb by Tonic and Activity-Dependent Presynaptic Inhibition of Receptor Neurons

Activation of Postsynaptic GABABReceptors Modulates the Bursting Pattern and Synaptic Activity of Olfactory Bulb Juxtaglomerular Neurons

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Activation of Postsynaptic GABA_BReceptors Modulates the Bursting Pattern and Synaptic Activity of Olfactory Bulb Juxtaglomerular Neurons