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The Journal of Neuroscience, June 18, 2008, 28(25):6360-6371; doi:10.1523/JNEUROSCI.0793-08.2008

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

Nicolás Pírez and Matt Wachowiak

Department of Biology, Boston University, Boston, Massachusetts 02215

Correspondence should be addressed to Dr. Matt Wachowiak, Department of Biology, Boston University, 5 Cummington Street, Boston, MA 02215. Email: dmattw{at}bu.edu

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.

Key words: calcium; GABAergic modulation; olfactory bulb; optical imaging; presynaptic regulation; sensory neurons

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Received Feb. 21, 2008; revised May 6, 2008; accepted May 7, 2008.

Correspondence should be addressed to Dr. Matt Wachowiak, Department of Biology, Boston University, 5 Cummington Street, Boston, MA 02215. Email: dmattw{at}bu.edu

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