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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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Pheromone-evoked spiking activities are qualitatively and quantitatively different in ORNs and PNs.In this and all following figures ORNs are shown in blue and PNs in red. (A) Phasic-tonic activity in a single ORN at various doses C of Z7-12∶Ac from -1 to 4 log ng (bar: stimulus duration, 200 ms). Schematic representation based on spike sorting. Hexane (hex) used as control. Vertical line at Tt = 180±13 ms (mean ± SD) indicates mean time of arrival of stimulus on antenna. (B) Multiphasic activity in a PN at doses from -3 to 1 with repetitions. Same representation as in (A). (C) Instantaneous firing rates estimated with a 50 ms Gaussian kernel (see Methods) of spike trains shown in (A). (D) Instantaneous firing rates of the trains shown in (B). (E) Comparison of average instantaneous firing rates of ORNs and PNs recorded at doses -1, 0 and 1 log ng. (F) Firing rate F versus latency L pairs from the same pheromone-evoked response for all ORNs (blue) and PNs (red) recorded at dose C = −1 log ng (responses significantly different shown as filled circles; all other figures show only responses significantly different from spontaneous activity).
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pcbi-1003975-g002: Pheromone-evoked spiking activities are qualitatively and quantitatively different in ORNs and PNs.In this and all following figures ORNs are shown in blue and PNs in red. (A) Phasic-tonic activity in a single ORN at various doses C of Z7-12∶Ac from -1 to 4 log ng (bar: stimulus duration, 200 ms). Schematic representation based on spike sorting. Hexane (hex) used as control. Vertical line at Tt = 180±13 ms (mean ± SD) indicates mean time of arrival of stimulus on antenna. (B) Multiphasic activity in a PN at doses from -3 to 1 with repetitions. Same representation as in (A). (C) Instantaneous firing rates estimated with a 50 ms Gaussian kernel (see Methods) of spike trains shown in (A). (D) Instantaneous firing rates of the trains shown in (B). (E) Comparison of average instantaneous firing rates of ORNs and PNs recorded at doses -1, 0 and 1 log ng. (F) Firing rate F versus latency L pairs from the same pheromone-evoked response for all ORNs (blue) and PNs (red) recorded at dose C = −1 log ng (responses significantly different shown as filled circles; all other figures show only responses significantly different from spontaneous activity).

Mentions: When stimulated with the components of the pheromone, the cumulus of the male moth Agrotis ipsilon was activated only by the main pheromone component, cis-7-dodecenyl acetate (Z7-12:Ac) (Fig. 1A). Conversely, the other glomeruli in the MGC were activated only by the other pheromone components (Fig. 1B–C). In electrophysiological recordings, the Z7-12:Ac-responsive ORNs displayed phasic-tonic responses (Fig. 2A, C) whereas the second-order neurons we studied shared a common multiphasic response pattern with an initial excitation followed by an inhibition (Fig. 2B, D) and frequently a final rebound (Fig. 2E). All stained multiphasic neurons were found to be PNs with dendritic trees in the cumulus and axons in the inner antenno-cerebral tract. The rare stained LNs we found (3 among 67 stained cells) were monophasic. Although these observations do not rule out the existence of LNs with a multiphasic response pattern, they support the contention that multiphasic LNs (if they exist) are rare in our recording conditions, which means that most if not all recorded neurons were PNs. For this reason, in the following, we used the more common term PN.


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)

Pheromone-evoked spiking activities are qualitatively and quantitatively different in ORNs and PNs.In this and all following figures ORNs are shown in blue and PNs in red. (A) Phasic-tonic activity in a single ORN at various doses C of Z7-12∶Ac from -1 to 4 log ng (bar: stimulus duration, 200 ms). Schematic representation based on spike sorting. Hexane (hex) used as control. Vertical line at Tt = 180±13 ms (mean ± SD) indicates mean time of arrival of stimulus on antenna. (B) Multiphasic activity in a PN at doses from -3 to 1 with repetitions. Same representation as in (A). (C) Instantaneous firing rates estimated with a 50 ms Gaussian kernel (see Methods) of spike trains shown in (A). (D) Instantaneous firing rates of the trains shown in (B). (E) Comparison of average instantaneous firing rates of ORNs and PNs recorded at doses -1, 0 and 1 log ng. (F) Firing rate F versus latency L pairs from the same pheromone-evoked response for all ORNs (blue) and PNs (red) recorded at dose C = −1 log ng (responses significantly different shown as filled circles; all other figures show only responses significantly different from spontaneous activity).
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pcbi-1003975-g002: Pheromone-evoked spiking activities are qualitatively and quantitatively different in ORNs and PNs.In this and all following figures ORNs are shown in blue and PNs in red. (A) Phasic-tonic activity in a single ORN at various doses C of Z7-12∶Ac from -1 to 4 log ng (bar: stimulus duration, 200 ms). Schematic representation based on spike sorting. Hexane (hex) used as control. Vertical line at Tt = 180±13 ms (mean ± SD) indicates mean time of arrival of stimulus on antenna. (B) Multiphasic activity in a PN at doses from -3 to 1 with repetitions. Same representation as in (A). (C) Instantaneous firing rates estimated with a 50 ms Gaussian kernel (see Methods) of spike trains shown in (A). (D) Instantaneous firing rates of the trains shown in (B). (E) Comparison of average instantaneous firing rates of ORNs and PNs recorded at doses -1, 0 and 1 log ng. (F) Firing rate F versus latency L pairs from the same pheromone-evoked response for all ORNs (blue) and PNs (red) recorded at dose C = −1 log ng (responses significantly different shown as filled circles; all other figures show only responses significantly different from spontaneous activity).
Mentions: When stimulated with the components of the pheromone, the cumulus of the male moth Agrotis ipsilon was activated only by the main pheromone component, cis-7-dodecenyl acetate (Z7-12:Ac) (Fig. 1A). Conversely, the other glomeruli in the MGC were activated only by the other pheromone components (Fig. 1B–C). In electrophysiological recordings, the Z7-12:Ac-responsive ORNs displayed phasic-tonic responses (Fig. 2A, C) whereas the second-order neurons we studied shared a common multiphasic response pattern with an initial excitation followed by an inhibition (Fig. 2B, D) and frequently a final rebound (Fig. 2E). All stained multiphasic neurons were found to be PNs with dendritic trees in the cumulus and axons in the inner antenno-cerebral tract. The rare stained LNs we found (3 among 67 stained cells) were monophasic. Although these observations do not rule out the existence of LNs with a multiphasic response pattern, they support the contention that multiphasic LNs (if they exist) are rare in our recording conditions, which means that most if not all recorded neurons were PNs. For this reason, in the following, we used the more common term PN.

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