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Efficient olfactory coding in the pheromone receptor neuron of a moth.

Kostal L, Lansky P, Rospars JP - PLoS Comput. Biol. (2008)

Bottom Line: Encouraged by the successful invocation of this principle to predict how neurons encode natural auditory and visual stimuli, we attempted its application to olfactory neurons.These results should stimulate further quantitative studies on the evolutionary adaptation of olfactory nervous systems to odorant plumes and on the plume characteristics that are most informative for the 'sniffer'.Both aspects are relevant to the design of olfactory sensors for odour-tracking robots.

View Article: PubMed Central - PubMed

Affiliation: Institute of Physiology, Academy of Sciences, Prague, Czech Republic.

ABSTRACT
The concept of coding efficiency holds that sensory neurons are adapted, through both evolutionary and developmental processes, to the statistical characteristics of their natural stimulus. Encouraged by the successful invocation of this principle to predict how neurons encode natural auditory and visual stimuli, we attempted its application to olfactory neurons. The pheromone receptor neuron of the male moth Antheraea polyphemus, for which quantitative properties of both the natural stimulus and the reception processes are available, was selected. We predicted several characteristics that the pheromone plume should possess under the hypothesis that the receptors perform optimally, i.e., transfer as much information on the stimulus per unit time as possible. Our results demonstrate that the statistical characteristics of the predicted stimulus, e.g., the probability distribution function of the stimulus concentration, the spectral density function of the stimulation course, and the intermittency, are in good agreement with those measured experimentally in the field. These results should stimulate further quantitative studies on the evolutionary adaptation of olfactory nervous systems to odorant plumes and on the plume characteristics that are most informative for the 'sniffer'. Both aspects are relevant to the design of olfactory sensors for odour-tracking robots.

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Related in: MedlinePlus

Visualization of a pheromone plume.The figure is extracted and adapted from a digitized image of a smoke plume filmed in a wind tunnel 1 m across and 2 m long with source on the left side [43]. Though the average pheromone concentration in the air decreases with distance, high pheromone concentrations can be found relatively far from the source due to the imperfect mixing of odorant with air. The signal detected by both moving and stationary detectors is therefore always intermittent, consisting of pulses of relatively undiluted pheromone.
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pcbi-1000053-g002: Visualization of a pheromone plume.The figure is extracted and adapted from a digitized image of a smoke plume filmed in a wind tunnel 1 m across and 2 m long with source on the left side [43]. Though the average pheromone concentration in the air decreases with distance, high pheromone concentrations can be found relatively far from the source due to the imperfect mixing of odorant with air. The signal detected by both moving and stationary detectors is therefore always intermittent, consisting of pulses of relatively undiluted pheromone.

Mentions: Flying male moths rely on the detection of pheromone molecules released by immobile conspecific females for mating. The atmospheric turbulence causes strong mixing of the air and creates a wide spectrum of spatio-temporal variations in the pheromonal signal (Figure 2). The largest eddies are hundreds of metres in size and may take minutes to pass a fixed point, while the smallest spatial variations are less than a millimetre in size and last for milliseconds only [15],[16]. Due to inhomogeneous mixing, a very high concentration of pheromone can be found in a wide range of distances from the source, though their frequency decreases with distance [15]. Because of its complicated and inhomogeneous structure, the description of the plume must rely on statistical methods, notably the histogram of the fluctuations in pheromone concentration [15]–[19]. These fluctuations are essential for the insect to locate the source of the stimulus. Experiments in wind tunnels showed that moths would not fly upwind in a uniform cloud of pheromone [20]–[22]. Characteristics like the frequency and intensity of the intermittent stimulation play a key role in maintaining the proper direction of flight [23].


Efficient olfactory coding in the pheromone receptor neuron of a moth.

Kostal L, Lansky P, Rospars JP - PLoS Comput. Biol. (2008)

Visualization of a pheromone plume.The figure is extracted and adapted from a digitized image of a smoke plume filmed in a wind tunnel 1 m across and 2 m long with source on the left side [43]. Though the average pheromone concentration in the air decreases with distance, high pheromone concentrations can be found relatively far from the source due to the imperfect mixing of odorant with air. The signal detected by both moving and stationary detectors is therefore always intermittent, consisting of pulses of relatively undiluted pheromone.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2291565&req=5

pcbi-1000053-g002: Visualization of a pheromone plume.The figure is extracted and adapted from a digitized image of a smoke plume filmed in a wind tunnel 1 m across and 2 m long with source on the left side [43]. Though the average pheromone concentration in the air decreases with distance, high pheromone concentrations can be found relatively far from the source due to the imperfect mixing of odorant with air. The signal detected by both moving and stationary detectors is therefore always intermittent, consisting of pulses of relatively undiluted pheromone.
Mentions: Flying male moths rely on the detection of pheromone molecules released by immobile conspecific females for mating. The atmospheric turbulence causes strong mixing of the air and creates a wide spectrum of spatio-temporal variations in the pheromonal signal (Figure 2). The largest eddies are hundreds of metres in size and may take minutes to pass a fixed point, while the smallest spatial variations are less than a millimetre in size and last for milliseconds only [15],[16]. Due to inhomogeneous mixing, a very high concentration of pheromone can be found in a wide range of distances from the source, though their frequency decreases with distance [15]. Because of its complicated and inhomogeneous structure, the description of the plume must rely on statistical methods, notably the histogram of the fluctuations in pheromone concentration [15]–[19]. These fluctuations are essential for the insect to locate the source of the stimulus. Experiments in wind tunnels showed that moths would not fly upwind in a uniform cloud of pheromone [20]–[22]. Characteristics like the frequency and intensity of the intermittent stimulation play a key role in maintaining the proper direction of flight [23].

Bottom Line: Encouraged by the successful invocation of this principle to predict how neurons encode natural auditory and visual stimuli, we attempted its application to olfactory neurons.These results should stimulate further quantitative studies on the evolutionary adaptation of olfactory nervous systems to odorant plumes and on the plume characteristics that are most informative for the 'sniffer'.Both aspects are relevant to the design of olfactory sensors for odour-tracking robots.

View Article: PubMed Central - PubMed

Affiliation: Institute of Physiology, Academy of Sciences, Prague, Czech Republic.

ABSTRACT
The concept of coding efficiency holds that sensory neurons are adapted, through both evolutionary and developmental processes, to the statistical characteristics of their natural stimulus. Encouraged by the successful invocation of this principle to predict how neurons encode natural auditory and visual stimuli, we attempted its application to olfactory neurons. The pheromone receptor neuron of the male moth Antheraea polyphemus, for which quantitative properties of both the natural stimulus and the reception processes are available, was selected. We predicted several characteristics that the pheromone plume should possess under the hypothesis that the receptors perform optimally, i.e., transfer as much information on the stimulus per unit time as possible. Our results demonstrate that the statistical characteristics of the predicted stimulus, e.g., the probability distribution function of the stimulus concentration, the spectral density function of the stimulation course, and the intermittency, are in good agreement with those measured experimentally in the field. These results should stimulate further quantitative studies on the evolutionary adaptation of olfactory nervous systems to odorant plumes and on the plume characteristics that are most informative for the 'sniffer'. Both aspects are relevant to the design of olfactory sensors for odour-tracking robots.

Show MeSH
Related in: MedlinePlus