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Heterogeneity and convergence of olfactory first-order neurons account for the high speed and sensitivity of second-order neurons.

Rospars JP, Grémiaux A, Jarriault D, Chaffiol A, Monsempes C, Deisig N, Anton S, Lucas P, Martinez D - PLoS Comput. Biol. (2014)

Bottom Line: We found that over all their dynamic range, PNs respond with a shorter latency and a higher firing rate than most ORNs.So, far from being detrimental to signal detection, the ORN heterogeneity is exploited by PNs, and results in two different schemes of population coding based either on the response of a few extreme neurons (latency) or on the average response of many (firing rate).Moreover, ORN-to-PN transformations are linear for latency and nonlinear for firing rate, suggesting that latency could be involved in concentration-invariant coding of the pheromone blend and that sensitivity at low concentrations is achieved at the expense of precise encoding at high concentrations.

View Article: PubMed Central - PubMed

Affiliation: Institut National de la Recherche Agronomique (INRA), Unité Mixte de Recherche 1392 Institut d'Ecologie et des Sciences de l'Environnement de Paris, Versailles, France.

ABSTRACT
In the olfactory system of male moths, a specialized subset of neurons detects and processes the main component of the sex pheromone emitted by females. It is composed of several thousand first-order olfactory receptor neurons (ORNs), all expressing the same pheromone receptor, that contact synaptically a few tens of second-order projection neurons (PNs) within a single restricted brain area. The functional simplicity of this system makes it a favorable model for studying the factors that contribute to its exquisite sensitivity and speed. Sensory information--primarily the identity and intensity of the stimulus--is encoded as the firing rate of the action potentials, and possibly as the latency of the neuron response. We found that over all their dynamic range, PNs respond with a shorter latency and a higher firing rate than most ORNs. Modelling showed that the increased sensitivity of PNs can be explained by the ORN-to-PN convergent architecture alone, whereas their faster response also requires cell-to-cell heterogeneity of the ORN population. So, far from being detrimental to signal detection, the ORN heterogeneity is exploited by PNs, and results in two different schemes of population coding based either on the response of a few extreme neurons (latency) or on the average response of many (firing rate). Moreover, ORN-to-PN transformations are linear for latency and nonlinear for firing rate, suggesting that latency could be involved in concentration-invariant coding of the pheromone blend and that sensitivity at low concentrations is achieved at the expense of precise encoding at high concentrations.

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Spontaneous activity in PNs is higher than in ORNs and depends on ORN spontaneous activity.(A) Total number of spontaneous spikes Nsp fired from time 0 to ti (firing time of ith spike) plotted as a function of ti in 4 ORNs (blue) and 4 PNs (red). The mean spontaneous firing rate is the slope of the regression line of Nsp vs. t. (B) Spontaneous activity of a PN before and after sectioning the antennal nerve (black cross); same representation as in (A). Top curve: first 3 min with sectioning marked with cross; slope of regression line before sectioning  = 32 AP/s. Bottom curve: same neuron from 5 to 8 min after sectioning (slope  = 5.6 AP/s). (C) Distribution of spontaneous firing rates in ORNs (blue) and PNs (red), with empirical cumulative distribution functions (CDFs, staircase), fitted lognormal CDFs (dashed curve) and corresponding probability distribution functions (PDFs, dotted curve). Parameters of these distributions are given in S2 Table.
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pcbi-1003975-g003: Spontaneous activity in PNs is higher than in ORNs and depends on ORN spontaneous activity.(A) Total number of spontaneous spikes Nsp fired from time 0 to ti (firing time of ith spike) plotted as a function of ti in 4 ORNs (blue) and 4 PNs (red). The mean spontaneous firing rate is the slope of the regression line of Nsp vs. t. (B) Spontaneous activity of a PN before and after sectioning the antennal nerve (black cross); same representation as in (A). Top curve: first 3 min with sectioning marked with cross; slope of regression line before sectioning  = 32 AP/s. Bottom curve: same neuron from 5 to 8 min after sectioning (slope  = 5.6 AP/s). (C) Distribution of spontaneous firing rates in ORNs (blue) and PNs (red), with empirical cumulative distribution functions (CDFs, staircase), fitted lognormal CDFs (dashed curve) and corresponding probability distribution functions (PDFs, dotted curve). Parameters of these distributions are given in S2 Table.

Mentions: Even in the absence of pheromone delivery, the Z7-12:Ac-responsive ORNs and PNs spiked tonically. This spontaneous activity is stationary (Fig. 3A) with a median firing rate lower in ORNs than in PNs (Fig. 3A, C). The distributions of spontaneous firing rates Fsp (all symbols are defined in S1 Table) are well fitted to lognormal distributions with a longer tail in PNs than in ORNs (Fig. 3C; S2 Table). To determine whether the PN activity is influenced by ORNs at rest, the antenna was sectioned. The PN firing rate began to decrease ∼10 s after the section and reached a stable regime (∼70% lower, range 58-85%) after less than 5 min (Fig. 3B).


Heterogeneity and convergence of olfactory first-order neurons account for the high speed and sensitivity of second-order neurons.

Rospars JP, Grémiaux A, Jarriault D, Chaffiol A, Monsempes C, Deisig N, Anton S, Lucas P, Martinez D - PLoS Comput. Biol. (2014)

Spontaneous activity in PNs is higher than in ORNs and depends on ORN spontaneous activity.(A) Total number of spontaneous spikes Nsp fired from time 0 to ti (firing time of ith spike) plotted as a function of ti in 4 ORNs (blue) and 4 PNs (red). The mean spontaneous firing rate is the slope of the regression line of Nsp vs. t. (B) Spontaneous activity of a PN before and after sectioning the antennal nerve (black cross); same representation as in (A). Top curve: first 3 min with sectioning marked with cross; slope of regression line before sectioning  = 32 AP/s. Bottom curve: same neuron from 5 to 8 min after sectioning (slope  = 5.6 AP/s). (C) Distribution of spontaneous firing rates in ORNs (blue) and PNs (red), with empirical cumulative distribution functions (CDFs, staircase), fitted lognormal CDFs (dashed curve) and corresponding probability distribution functions (PDFs, dotted curve). Parameters of these distributions are given in S2 Table.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4256018&req=5

pcbi-1003975-g003: Spontaneous activity in PNs is higher than in ORNs and depends on ORN spontaneous activity.(A) Total number of spontaneous spikes Nsp fired from time 0 to ti (firing time of ith spike) plotted as a function of ti in 4 ORNs (blue) and 4 PNs (red). The mean spontaneous firing rate is the slope of the regression line of Nsp vs. t. (B) Spontaneous activity of a PN before and after sectioning the antennal nerve (black cross); same representation as in (A). Top curve: first 3 min with sectioning marked with cross; slope of regression line before sectioning  = 32 AP/s. Bottom curve: same neuron from 5 to 8 min after sectioning (slope  = 5.6 AP/s). (C) Distribution of spontaneous firing rates in ORNs (blue) and PNs (red), with empirical cumulative distribution functions (CDFs, staircase), fitted lognormal CDFs (dashed curve) and corresponding probability distribution functions (PDFs, dotted curve). Parameters of these distributions are given in S2 Table.
Mentions: Even in the absence of pheromone delivery, the Z7-12:Ac-responsive ORNs and PNs spiked tonically. This spontaneous activity is stationary (Fig. 3A) with a median firing rate lower in ORNs than in PNs (Fig. 3A, C). The distributions of spontaneous firing rates Fsp (all symbols are defined in S1 Table) are well fitted to lognormal distributions with a longer tail in PNs than in ORNs (Fig. 3C; S2 Table). To determine whether the PN activity is influenced by ORNs at rest, the antenna was sectioned. The PN firing rate began to decrease ∼10 s after the section and reached a stable regime (∼70% lower, range 58-85%) after less than 5 min (Fig. 3B).

Bottom Line: We found that over all their dynamic range, PNs respond with a shorter latency and a higher firing rate than most ORNs.So, far from being detrimental to signal detection, the ORN heterogeneity is exploited by PNs, and results in two different schemes of population coding based either on the response of a few extreme neurons (latency) or on the average response of many (firing rate).Moreover, ORN-to-PN transformations are linear for latency and nonlinear for firing rate, suggesting that latency could be involved in concentration-invariant coding of the pheromone blend and that sensitivity at low concentrations is achieved at the expense of precise encoding at high concentrations.

View Article: PubMed Central - PubMed

Affiliation: Institut National de la Recherche Agronomique (INRA), Unité Mixte de Recherche 1392 Institut d'Ecologie et des Sciences de l'Environnement de Paris, Versailles, France.

ABSTRACT
In the olfactory system of male moths, a specialized subset of neurons detects and processes the main component of the sex pheromone emitted by females. It is composed of several thousand first-order olfactory receptor neurons (ORNs), all expressing the same pheromone receptor, that contact synaptically a few tens of second-order projection neurons (PNs) within a single restricted brain area. The functional simplicity of this system makes it a favorable model for studying the factors that contribute to its exquisite sensitivity and speed. Sensory information--primarily the identity and intensity of the stimulus--is encoded as the firing rate of the action potentials, and possibly as the latency of the neuron response. We found that over all their dynamic range, PNs respond with a shorter latency and a higher firing rate than most ORNs. Modelling showed that the increased sensitivity of PNs can be explained by the ORN-to-PN convergent architecture alone, whereas their faster response also requires cell-to-cell heterogeneity of the ORN population. So, far from being detrimental to signal detection, the ORN heterogeneity is exploited by PNs, and results in two different schemes of population coding based either on the response of a few extreme neurons (latency) or on the average response of many (firing rate). Moreover, ORN-to-PN transformations are linear for latency and nonlinear for firing rate, suggesting that latency could be involved in concentration-invariant coding of the pheromone blend and that sensitivity at low concentrations is achieved at the expense of precise encoding at high concentrations.

Show MeSH
Related in: MedlinePlus