Plasticity of local GABAergic interneurons drives olfactory habituation
Open Access
- 27 July 2011
- journal article
- research article
- Published by Proceedings of the National Academy of Sciences in Proceedings of the National Academy of Sciences of the United States of America
- Vol. 108 (36), E646-E654
- https://doi.org/10.1073/pnas.1106411108
Abstract
Despite its ubiquity and significance, behavioral habituation is poorly understood in terms of the underlying neural circuit mechanisms. Here, we present evidence that habituation arises from potentiation of inhibitory transmission within a circuit motif commonly repeated in the nervous system. In Drosophila, prior odorant exposure results in a selective reduction of response to this odorant. Both short-term (STH) and long-term (LTH) forms of olfactory habituation require function of the rutabaga-encoded adenylate cyclase in multiglomerular local interneurons (LNs) that mediate GABAergic inhibition in the antennal lobe; LTH additionally requires function of the cAMP response element-binding protein (CREB2) transcription factor in LNs. The odorant selectivity of STH and LTH is mirrored by requirement for NMDA receptors and GABAA receptors in odorant-selective, glomerulus-specific projection neurons(PNs). The need for the vesicular glutamate transporter in LNs indicates that a subset of these GABAergic neurons also releases glutamate. LTH is associated with a reduction of odorant-evoked calcium fluxes in PNs as well as growth of the respective odorant-responsive glomeruli. These cellular changes use similar mechanisms to those required for behavioral habituation. Taken together with the observation that enhancement of GABAergic transmission is sufficient to attenuate olfactory behavior, these data indicate that habituation arises from glomerulus-selective potentiation of inhibitory synapses in the antennal lobe. We suggest that similar circuit mechanisms may operate in other species and sensory systems.Keywords
This publication has 66 references indexed in Scilit:
- Long-term plasticity at inhibitory synapsesCurrent Opinion in Neurobiology, 2011
- Presynaptic Facilitation by Neuropeptide Signaling Mediates Odor-Driven Food SearchCell, 2011
- Electrical Coupling between Olfactory GlomeruliNeuron, 2010
- A Neural Circuit Mechanism Integrating Motivational State with Memory Expression in DrosophilaCell, 2009
- Olfactory Perception: Receptors, Cells, and CircuitsCell, 2009
- Habituation revisited: An updated and revised description of the behavioral characteristics of habituationNeurobiology of Learning and Memory, 2009
- Neurogenetic approaches to habituation and dishabituation in DrosophilaNeurobiology of Learning and Memory, 2009
- Short- and Long-Term Memory in Drosophila Require cAMP Signaling in Distinct Neuron TypesCurrent Biology, 2009
- A Presynaptic Gain Control Mechanism Fine-Tunes Olfactory BehaviorNeuron, 2008
- Excitatory Local Circuits and Their Implications for Olfactory Processing in the Fly Antennal LobeCell, 2007