Contrast enhancement of stimulus intermittency in a primary olfactory network and its behavioral significance

University of Arizona, Tucson, 85721-0077, USA.
Journal of Biology 03/2009; 8(2):21. DOI: 10.1186/jbiol120
Source: PubMed


An animal navigating to an unseen odor source must accurately resolve the spatiotemporal distribution of that stimulus in order to express appropriate upwind flight behavior. Intermittency of natural odor plumes, caused by air turbulence, is critically important for many insects, including the hawkmoth, Manduca sexta, for odor-modulated search behavior to an odor source. When a moth's antennae receive intermittent odor stimulation, the projection neurons (PNs) in the primary olfactory centers (the antennal lobes), which are analogous to the olfactory bulbs of vertebrates, generate discrete bursts of action potentials separated by periods of inhibition, suggesting that the PNs may use the binary burst/non-burst neural patterns to resolve and enhance the intermittency of the stimulus encountered in the odor plume.
We tested this hypothesis first by establishing that bicuculline methiodide reliably and reversibly disrupted the ability of PNs to produce bursting response patterns. Behavioral studies, in turn, demonstrated that after injecting this drug into the antennal lobe at the effective concentration used in the physiological experiments animals could no longer efficiently locate the odor source, even though they had detected the odor signal.
Our results establish a direct link between the bursting response pattern of PNs and the odor-tracking behavior of the moth, demonstrating the behavioral significance of resolving the dynamics of a natural odor stimulus in antennal lobe circuits.

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Available from: Hong Lei, Oct 04, 2015
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    • "However, the transient oscillatory synchronization does not appear to play a role in odor discrimination in M. sexta (Mwilaria et al., 2008; Daly et al., 2011). Alternatively, it has been proposed that odor drives “onset” synchronization of the output response from primary olfactory centers allowing the AL to track the time varying concentration of the plume structure (Christensen et al., 2003; Lei et al., 2009). We have argued that odor dependent representations are correlated to a sequence of onset latencies from different subsets of synchronously active AL outputs that evolve over and are optimized within <150 ms (Daly et al., 2004b; Staudacher et al., 2009). "
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    ABSTRACT: Animals use behaviors to actively sample the environment across a broad spectrum of sensory domains. These behaviors discretize the sensory experience into unique spatiotemporal moments, minimize sensory adaptation, and enhance perception. In olfaction, behaviors such as sniffing, antennal flicking, and wing beating all act to periodically expose olfactory epithelium. In mammals, it is thought that sniffing enhances neural representations; however, the effects of insect wing beating on representations remain unknown. To determine how well the antennal lobe (AL) produces odor dependent representations when wing beating effects are simulated, we used extracellular methods to record neural units and local field potentials (LFPs) from moth AL. We recorded responses to odors presented as prolonged continuous stimuli or periodically as 20 and 25 Hz pulse trains designed to simulate the oscillating effects of wing beating around the antennae during odor guided flight. Using spectral analyses, we show that ~25% of all recorded units were able to entrain to "pulsed stimuli"; this includes pulsed blanks, which elicited the strongest overall entrainment. The strength of entrainment to pulse train stimuli was dependent on molecular features of the odorants, odor concentration, and pulse train duration. Moreover, units showing pulse tracking responses were highly phase locked to LFPs during odor stimulation, indicating that unit-LFP phase relationships are stimulus-driven. Finally, a Euclidean distance-based population vector analysis established that AL odor representations are more robust, peak more quickly, and do not show adaptation when odors were presented at the natural wing beat frequency as opposed to prolonged continuous stimulation. These results suggest a general strategy for optimizing olfactory representations, which exploits the natural rhythmicity of wing beating by integrating mechanosensory and olfactory cues at the level of the AL.
    Frontiers in Cellular Neuroscience 06/2014; 8:159. DOI:10.3389/fncel.2014.00159 · 4.29 Impact Factor
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    • "Drug delivery into the ALs was accomplished via a microinjection surgery (Lei et al., 2009; Gage et al., 2013). Animals were restrained in a plastic tube, and an hourglass window was cut into the head capsule. "
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    ABSTRACT: Nitric oxide (NO) is thought to play an important neuromodulatory role in the olfactory system. This modulation has been suggested to be particularly important for olfactory learning and memory in the antennal lobe (the primary olfactory network in invertebrates). We are using the hawkmoth, Manduca sexta, to further investigate the role of NO in olfactory memory. Recent findings suggest that NO affects short-term memory traces and that NO concentration fluctuates with the light cycle. This gives rise to the hypothesis that NO may be involved in the connection between memory and circadian rhythms. In this study, we explore the role of diurnal time and NO in memory by altering the time of day when associative-olfactory conditioning is performed. We find a strong effect of NO on short-term memory, and two surprising effects of diurnal time. We find that (1) at certain time points, NO affects longer traces of memory in addition to short-term memory; and (2) when conditioning is performed close to the light cycle switches—both from light to dark and dark to light—NO does not significantly affect memory at all. These findings suggest an intriguing functional role for NO in olfactory conditioning that is modulated as a function of diurnal time.
    Frontiers in Systems Neuroscience 04/2014; 8(1). DOI:10.3389/fnsys.2014.00059
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    • "Therefore, an alternative and more plausible function of inhibition is an involvement in the control of temporal response patterns of PNs, that become important when encountering pulse trains of odorant stimuli, as present under natural conditions. The involvement of inhibition in shortening response durations has previously been demonstrated in the sphinx moth, Manduca sexta [43]–[46]. We have now shown that inhibition involved in response shortening acts downstream of the ORN-PN synapses and in a concentration-dependent manner. "
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    ABSTRACT: Although odorant concentration-response characteristics of olfactory neurons have been widely investigated in a variety of animal species, the effect of odorant concentration on neural processing at circuit level is still poorly understood. Using calcium imaging in the silkmoth (Bombyx mori) pheromone processing circuit of the antennal lobe (AL), we studied the effect of odorant concentration on second-order projection neuron (PN) responses. While PN calcium responses of dendrites showed monotonic increases with odorant concentration, calcium responses of somata showed decreased responses at higher odorant concentrations due to postsynaptic inhibition. Simultaneous calcium imaging and electrophysiology revealed that calcium responses of PN somata but not dendrites reflect spiking activity. Inhibition shortened spike response duration rather than decreasing peak instantaneous spike frequency (ISF). Local interneurons (LNs) that were specifically activated at high odorant concentrations at which PN responses were suppressed are the putative source of inhibition. Our results imply the existence of an intraglomerular mechanism that preserves time resolution in olfactory processing over a wide odorant concentration range.
    PLoS ONE 02/2014; 9(2):e89132. DOI:10.1371/journal.pone.0089132 · 3.23 Impact Factor
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