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

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

Brain Research Bulletin

Volume 35, Issue 2, 1994, Pages 119-123

https://doi.org/10.1016/0361-9230(94)90091-4 Get rights and content

Abstract

The GABA_B agonist baclofen blocks transmission from the olfactory nerve to second order neurons in the frog olfactory bulb, and GABA_B receptors in the rat olfactory bulb are selectively located in the glomerular layer. A reasonable hypothesis, therefore, is that inhibition in the glomerular layer is mediated, at least in part, by GABA_B receptors. Here, we investigated the role of GABA_B receptors in regulating the responses of mitral cells to activation of the olfactory nerve in the rat. Topical application of baclofen to the surface of the rat olfactory bulb reduced the amplitude of field potentials evoked by olfactory nerve stimulation (orthodromic response). Baclofen reduced the orthodromic response in a dose-dependent manner but the drug had no effect on the field potential evoked by antidromic activation of mitral cell axons (antidromic response). Baclofen also reduced olfactory nerve-evoked responses of mitral cells in an olfactory bulb slice preparation. The pharmacological specificity of the inhibition was confirmed by showing that the GABA_B antagonist, CGP 55845A, blocked the inhibitory action of baclofen. These results suggest that transmission from olfactory nerve terminals to second order neurons is negatively regulated by periglomerular GABAergic interneurons; this inhibition is mediated, at least partially, by GABA_B receptors.

References (27)

N.G. Bowery et al.
GABA_A and GABA_B receptor site distribution in the rat central nervous system
Neuroscience
(1987)
W.J. Freeman
Attenuation of transmission through glomeruli of olfactory buolb on paired shock stimulation
Brain Res.
(1974)
W.J. Freeman
Relation of glomerular neuronal activity to glomerular transmission attenuation
Brain Res.
(1974)
T. Kosaka et al.
Coexistence of immunoreactivities for glutamate decarboxylase and tyrosine hydroxylase in some neurons in the periglomerular region of the rat main olfactory bulb: Possible coexistence of gamma-aminobutyric acid (GABA) and dopamine
Brain Res.
(1985)
E. Mugnaini et al.
Immunocytochemical localization of GABA neurons and dopamine neurons in the rat main and accessory olfactory bulbs
Neurosci. Lett.
(1984)
R. Andrade et al.
A G protein couples sertonin and GABA_B receptors to the same channels in hippocampus
Science
(1986)
B.H. Gahwiler et al.
GABA_B-receptor-activated K⁺ current in voltage-clamped CA3 pyramidal cells in hippocampal cultures
C.M. Gall et al.
Evidence for coexistence of GABA and dopamine in neurons of the rat olfactory bulb
J. Comp. Neurol.
(1987)
T.V. Getchell et al.
Short-axon cells in the olfactory bulb: Dendrodendritic synaptic interactions
J. Physiol.
(1975)
T.A. Harrison et al.
Olfactory bulb responses to odor stimulation: Analysis of response pattern and intensity relationships
J. Neurophysiol.
(1986)

C.E. Jahr et al.

Primary afferent depolarization in the in vitro frog olfactory bulb

J. Physiol.

(1981)

M. Lacey et al.

On the potassium conductance increase activated by GABA_B and dopamine D₂ receptors in rat substantia nigra neurones

J. Physiol.

(1988)

F. Macrides et al.

The olfactory bulb

Cited by (62)

Sensory-Evoked Intrinsic Optical Signals in the Olfactory Bulb Are Coupled to Glutamate Release and Uptake
2006, Neuron
Citation Excerpt :
Are IOS directly coupled to action potentials of afferent olfactory receptor neurons (ORNs) or do they require neurotransmitter release? In vitro studies show that DA D2 agonists (Coronas et al., 1997; Duchamp-Viret et al., 1997) and GABA-B agonists (Bonino et al., 1999; Koster et al., 1999; Duchamp-Viret et al., 2000) are capable of inhibiting electrically-evoked synaptic transmission from ORNs to M/TCs without affecting input action potentials (Nickell et al., 1994; Hsia et al., 1999; Wachowiak and Cohen, 1999; Aroniadou-Anderjaska et al., 2000; Berkowicz and Trombley, 2000; Ennis et al., 2001; Palouzier-Paulignan et al., 2002). These drugs mimic the action of DA and GABA release from JGCs by activating D2 and GABA-B receptors located on ORN terminals (McLean and Shipley, 1988; Coronas et al., 1997; Duchamp-Viret et al., 1997, 2000; Bonino et al., 1999; Koster et al., 1999; Gutierrez-Mecinas et al., 2005) and suppressing presynaptic Ca2+ influx and glutamate release (Hsia et al., 1999; Ennis et al., 2001; Wachowiak et al., 2005).
Functional imaging signals arise from metabolic and hemodynamic activity, but how these processes are related to the synaptic and electrical activity of neurons is not well understood. To provide insight into this issue, we used in vivo imaging and simultaneous local pharmacology to study how sensory-evoked neural activity leads to intrinsic optical signals (IOS) in the well-defined circuitry of the olfactory glomerulus. Odor-evoked IOS were tightly coupled to release of glutamate and were strongly modulated by activation of presynaptic dopamine and GABA-B receptors. Surprisingly, IOS were independent of postsynaptic transmission through ionotropic or metabotropic glutamate receptors, but instead were inhibited when uptake by astrocytic glutamate transporters was blocked. These data suggest that presynaptic glutamate release and uptake by astrocytes form a critical pathway through which neural activity is linked to metabolic processing and hence to functional imaging signals.
Presynaptic GABA<inf>B</inf> receptors inhibit vomeronasal nerve transmission to accessory olfactory bulb mitral cells
2023, Frontiers in Cellular Neuroscience
Optical manipulations reveal strong reciprocal inhibition but limited recurrent excitation within olfactory bulb glomeruli
2021, eNeuro
Unraveling the Role of Dopaminergic and Calretinin Interneurons in the Olfactory Bulb
2021, Frontiers in Neural Circuits
Stimulus Driven Functional Transformations in the Early Olfactory System
2021, Frontiers in Cellular Neuroscience
Maturation of the olfactory sensory neuron and its Cilia
2020, Chemical Senses

View all citing articles on Scopus

View full text

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

Abstract

Neuroscience

Brain Res.

Brain Res.

Brain Res.

Neurosci. Lett.

A G protein couples sertonin and GABAB receptors to the same channels in hippocampus

Science

GABAB-receptor-activated K+ current in voltage-clamped CA3 pyramidal cells in hippocampal cultures

Evidence for coexistence of GABA and dopamine in neurons of the rat olfactory bulb

J. Comp. Neurol.

Short-axon cells in the olfactory bulb: Dendrodendritic synaptic interactions

J. Physiol.

Olfactory bulb responses to odor stimulation: Analysis of response pattern and intensity relationships

J. Neurophysiol.

Primary afferent depolarization in the in vitro frog olfactory bulb

J. Physiol.

On the potassium conductance increase activated by GABAB and dopamine D2 receptors in rat substantia nigra neurones

J. Physiol.

The olfactory bulb

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

A G protein couples sertonin and GABA_B receptors to the same channels in hippocampus

GABA_B-receptor-activated K⁺ current in voltage-clamped CA3 pyramidal cells in hippocampal cultures

On the potassium conductance increase activated by GABA_B and dopamine D₂ receptors in rat substantia nigra neurones