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The Journal of Neuroscience, March 15, 2003, 23(6):2032

GABA_B Receptors Inhibit Dendrodendritic Transmission in the Rat Olfactory Bulb

Jeffry S. Isaacson and Harald Vitten

Department of Neuroscience, School of Medicine, University of California, San Diego, La Jolla, California 92093-0608

In the mammalian olfactory bulb, mitral cell dendrites release glutamate onto the dendritic spines of granule cells, which in turn release GABA back onto mitral dendrites. This local synaptic circuit forms the basis for reciprocal dendrodendritic inhibition mediated by ionotropic GABA_A receptors in mitral cells. Surprisingly little is known about neurotransmitter modulation of dendrodendritic signaling in the olfactory bulb. In this study, we examine whether metabotropic GABA_B receptors modulate dendrodendritic signaling between mitral and granule cells. We find that the selective GABA_B agonist baclofen reduces mitral cell recurrent inhibition mediated by dendrodendritic synapses. GABA_B receptor activation causes only a weak inhibition of field EPSCs in the external plexiform layer and only slightly reduces glutamate-mediated mitral cell self-excitation. Although GABA_B receptors depress mitral cell glutamate release only weakly, baclofen causes a marked reduction in the amplitude of granule-cell-evoked, GABA_A-mediated IPSCs in mitral cells. In addition to reducing the amplitude of granule-cell-evoked IPSCs, baclofen causes a change from paired-pulse depression to paired-pulse facilitation, suggesting that GABA_B receptors modulate GABA release from granule cells. To explore the mechanism of action of GABA_B receptors further, we show that baclofen inhibits high-voltage-activated calcium currents in granule cells. Together, these findings suggest that GABA_B receptors modulate dendrodendritic inhibition primarily by inhibiting granule cell calcium channels and reducing the release of GABA. Furthermore, we show that endogenous GABA regulates the strength of dendrodendritic inhibition via the activation of GABA_B autoreceptors.

Key words: GABA_B; baclofen; olfactory bulb; mitral cell; granule cell; dendrites; presynaptic; calcium channel

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Copyright © 2003 Society for Neuroscience  0270-6474/03/2362032-08$05.00/0

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