High-speed odor transduction and pulse tracking by insect olfactory receptor neurons

Abstract

Sensory systems encode both the static quality of a stimulus (e.g., color or shape) and its kinetics (e.g., speed and direction). The limits with which stimulus kinetics can be resolved are well understood in vision, audition, and somatosensation. However, the maximum temporal resolution of olfactory systems has not been accurately determined. Here, we probe the limits of temporal resolution in insect olfaction by delivering high frequency odor pulses and measuring sensory responses in the antennae. We show that transduction times and pulse tracking capabilities of olfactory receptor neurons are faster than previously reported. Once an odorant arrives at the boundary layer of the antenna, odor transduction can occur within less than 2 ms and fluctuating odor stimuli can be resolved at frequencies more than 100 Hz. Thus, insect olfactory receptor neurons can track stimuli of very short duration, as occur when their antennae encounter narrow filaments in an odor plume. These results provide a new upper bound to the kinetics of odor tracking in insect olfactory receptor neurons and to the latency of initial transduction events in olfaction.olfaction | olfactory receptor neurons | odor transduction | temporal resolution | insect O dors carried in air plumes quickly break up into thin filaments that spread out across short distances from an odor source (1). The ability to track the temporal structure of filaments in an odor plume is essential for insects to segregate concurrent odors that arise from different sources (2-6). However, it is not clear whether signal transduction times and tracking rates of olfactory receptor neurons (ORNs) are fast enough to allow animals to use the higher frequency components of information present in odor plumes. Insect odor-guided behavior is remarkably robust against the spatial and temporal variability inherent in olfactory stimuli. For example, moths and beetles use temporal stimulus cues to segregate concurrent odors from closely spaced sources (2-5), and honey bees can detect 6-ms asynchrony in the onset of concurrent odor stimuli and use this onset asynchrony to segregate concurrent odors (6, 7). These observations of fast temporal resolution challenge the frequent notion that olfaction has slow integration times relative to other senses. Olfactory transduction speed has never been measured directly, and estimates range from 10 to 30 ms (8-11). Previous studies suggest that the maximum pulse tracking frequency of ORNs is species specific and ranges from 5 to 50 Hz (12-19). However, these numbers do not match the high temporal resolution observed in behavioral studies (2-7).We tested the limits of olfactory transduction speed and pulse tracking in five different insect species by measuring ORN population responses using electroantennogram (EAG) recordings. The amplitude and dynamics of EAG signals are proportional to the number of sensilla stimulated (20). They are also affected by receptor current amplitude, positions of the neurons relative to the recording electrode, and elec...

Morphological characterization of the antennal lobes in the Mediterranean fruit fly Ceratitis capitata

“…The orientation of the AL is indicated by the crosses: A anterior, P posterior, D dorsal, V ventral, L lateral, M medial. The atlas is available as interactive 3D pdf file information across glomeruli may be important to process information in a fast, turbulent environment, as found in the insect world, and as reflected in fast olfactory receptor responses (Szyska et al 2014). Several electrical synapses have been found in D. melanogaster between local neurons and projection neurons, or among projection neurons (Yaksi and Wilson 2010;Wang et al 2014).…”

A Biophysical Model of the Early Olfactory System of Honeybees

“…Figure 6 shows the average ORN responses to 1-hexanol to square pulses of 2ms with different inter-pulse intervals and compares them to those measured by electro-antennogram recordings [9]. The model responses exhibit all relevant features observed in the experimental data except that the time scale of response latency is smaller.…”

“…In Section 2, we describe in details how our model was built. In Section 3, we show that our model reproduces key features of ORN and PN responses to continuous stimuli (3.1) and short pulses (3.2) observed in experimental work that was not considered when building the model [9,10,13,14]. In Section 4, we discuss the strength and limitations of our model and our plans for future work.…”

“…, 1 ( −1 ) and 2 ( −2 ) are partially constrained by the parameters in the Hill curves, which are statistically sampled in accordance to experimental observations in [8]. To deal with the remaining degrees of freedom, we took into account the typical timescale of dynamics in AL responses measured experimentally [9,10].…”

High-resolution Quantification of Odor-guided Behavior in <em>Drosophila melanogaster</em> Using the <em>Flywalk</em> Paradigm

“…Both walking and flying insects -including Drosophila-have been demonstrated to exploit this intermittent stimulation regime for navigation by surging upwind upon plume encounter and predominantly moving cross-wind in the absence of odors [2][3][4][5] . Whereas stimulation procedures in physiological experiments largely mimic those an insect may experience in its natural environment by either providing single puffs of odors interspersed with extended periods of clean air or dynamic stimulation sequences [6][7][8][9][10][11] , many behavioral bioassays used in Drosophila neuroethology such as trap assay, open-field arenas or T-maze rely on odor-gradients [12][13][14][15] . However, because odor gradients by definition are variable in concentration depending on the distance from the odor source, a particular behavior cannot be attributed to a precise odor concentration using these paradigms.…”