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Relationship between Afferent and Central Temporal Patterns in the Locust Olfactory System

Wehr, Michael and Laurent, Gilles (1999) Relationship between Afferent and Central Temporal Patterns in the Locust Olfactory System. Journal of Neuroscience, 19 (1). pp. 381-390. ISSN 0270-6474. PMCID PMC6782390. doi:10.1523/jneurosci.19-01-00381.1999.

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Odors evoke synchronized oscillations and slow temporal patterns in antennal lobe neurons and fast oscillations in the mushroom body local field potential (LFP) of the locust. What is the contribution of primary afferents in the generation of these dynamics? We addressed this question in two ways. First, we recorded odor-evoked afferent activity in both isolated antennae and intact preparations. Odor-evoked population activity in the antenna and the antennal nerve consisted of a slow potential deflection, similar for many odors. This deflection contained neither oscillatory nor odor-specific slow temporal patterns, whereas simultaneously recorded mushroom body LFPs exhibited clear 20–30 Hz oscillations. This suggests that the temporal patterning of antennal lobe and mushroom body neurons is generated downstream of the olfactory receptor axons. Second, we electrically stimulated arrays of primary afferents in vivo. A brief shock to the antennal nerve produced compound PSPs in antennal lobe projection neurons, with two peaks at an ∼50 msec interval. Prolonged afferent stimulation with step, ramp, or slow sine-shaped voltage waveforms evoked sustained 20–30 Hz oscillations in projection neuron membrane potential and in the mushroom body LFP. Projection neuron and mushroom body oscillations were phase-locked and reliable across trials. Synchronization of projection neurons was seen directly in paired intracellular recordings. Pressure injection of picrotoxin into the antennal lobe eliminated the oscillations evoked by electrical stimulation. Different projection neurons could express different temporal patterns in response to the same electrical stimulus, as seen for odor-evoked responses. Conversely, individual projection neurons could express different temporal patterns of activity in response to step stimulation of different spatial arrays of olfactory afferents. These patterns were reliable and remained distinct across different stimulus intensities. We conclude that oscillatory synchronization of olfactory neurons originates in the antennal lobe and that slow temporal patterns in projection neurons can arise in the absence of temporal patterning of the afferent input.

Item Type:Article
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URLURL TypeDescription CentralArticle
Laurent, Gilles0000-0002-2296-114X
Additional Information:© 1998 Society for Neuroscience. Received June 5, 1998; revised Sept. 14, 1998; accepted Oct. 13, 1998. This research was supported by a National Science Foundation grant and by National Institutes of Health and Howard Hughes Medical Institute training grants.
Funding AgencyGrant Number
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Subject Keywords:synchronization; oscillation; coding; olfactory receptors; olfaction; insect
Issue or Number:1
PubMed Central ID:PMC6782390
Record Number:CaltechAUTHORS:20191029-155743793
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Official Citation:Relationship between Afferent and Central Temporal Patterns in the Locust Olfactory System. Michael Wehr, Gilles Laurent. Journal of Neuroscience 1 January 1999, 19 (1) 381-390; DOI: 10.1523/JNEUROSCI.19-01-00381.1999
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:99549
Deposited By: Tony Diaz
Deposited On:29 Oct 2019 23:01
Last Modified:16 Nov 2021 17:47

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