Synchronous firing of antennal-lobe projection neurons encodes the behaviorally effective ratio of sex-pheromone components in male Manduca sexta

Martin, Joshua P.; Lei, Hong; Riffell, Jeffrey A.; Hildebrand, John G.

doi:10.1007/s00359-013-0849-z

Cited by 31 publications

(47 citation statements)

References 137 publications

(176 reference statements)

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“…At the peripheral level, it can be assumed that conditioning to B induces changes in firing rates of receptor cells activated by both odorants and/or the chemotopic pattern of B (Martin et al 2013). Moreover, the AB configural odor might compete and impair matching of afferent information with the previously acquired representation of B (Boyd et al 2012;Chapuis and Wilson 2011;Giessel and Datta 2014).…”

Section: Conditioning Effects On Mixture Perceptionmentioning

confidence: 99%

Brain processing of a configural vs elemental odor mixture in the newborn rabbit

et al. 2015

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Organisms are surrounded throughout life by chemically complex odors. How individuals process an odorant within a mixture or a mixture as a whole is a key question in neuroethology and chemical senses. This question is addressed here by using newborn rabbits, which can be rapidly conditioned to a new stimulus by single association with the mammary pheromone. After conditioning to ethyl maltol (odorant B), pups behaviorally respond to B and an A'B' mixture (68/32 ratio) but not to ethyl isobutyrate (odorant A) or an AB mixture (30/70 ratio). This suggests elemental and configural perception of A'B' and AB, respectively. We then explored the neural substrates underlying the processing of these mixtures with the hypothesis that processing varies according to perception. Pups were pseudoconditioned or conditioned to B on postnatal day 3 before exposure to B, A'B' or AB on day 4. Fos expression was not similar between groups (mainly in the olfactory bulb and posterior piriform cortex) suggesting a differential processing of the stimuli that might reflect either stimulus complexity or conditioning effect. Thus, the ratio of components in A'B' vs AB leads to differential activation of the olfactory system which may contribute to elemental and configural percepts of these mixtures. In addition, together with recent behavioral data, this highlights that configural perception occurs even in relatively immature animals, emphasizing the value of the newborn rabbit for exploration of odor mixture processing from molecules to brain and behavior.

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Section: Conditioning Effects On Mixture Perceptionmentioning

confidence: 99%

Brain processing of a configural vs elemental odor mixture in the newborn rabbit

et al. 2015

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“…Tumlinson et al 1989,1994; Vickers et al 2003; Domingue et al 2007, 2008; Kanno et al 2010; El-Sayed et al 2011; Leary et al 2012; Martin et al 2013), our finding that 24% of the sampled, pheromone-responsive protocerebral neurons in this study did not distinguish among the tested stimuli (supplemental Table 1) is surprising. Pairwise comparisons of responses to different pheromonal stimuli (EEZ vs. BAL, EEZ vs. mixture, BAL vs. mixture) showed that 50–80% of neurons exhibited no significant differences in their responses to these stimulus pairs (Figure 1, bottom).…”

Section: Discussionmentioning

confidence: 52%

“…These neurons could thus be considered as pheromone specialists. Moreover, within the behaviorally effective range of BAL:EEZ ratios (Martin et al 2013), 4 neurons (about 30% of the sample) gave strongest responses (white asterisks in Figure 5a) in comparison with their responses to other ratios or the two single components. Also noticeable was that about 50% of the sampled neurons exhibited response to the solvent control.…”

Section: Resultsmentioning

confidence: 95%

“…Most recently, using an extracellular recording method, Martin et al (2013, this issue) found that AL PNs associated with the male-specific macroglomerular complex in M. sexta show maximally synchronized spiking upon antennal stimulation with a mixture of the two key pheromone components, E 10- Z 12-hexadecadienal (bombykal or BAL, the major pheromone component of this species) and E 10- E 12- Z 14-hexadecatrienal (or EEZ, the second major component) at the natural 2:1 blend ratio. That synchronous activity decreases when the mixture ratio deviates from the natural 2:1.…”

Section: Introductionmentioning

confidence: 99%

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Responses of protocerebral neurons in Manduca sexta to sex-pheromone mixtures

2013

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Male Manduca sexta moths are attracted to a mixture of two components of the female's sex pheromone at the natural concentration ratio. Deviation from this ratio results in reduced attraction. Projection neurons innervating prominent male-specific glomeruli in the male's antennal lobe produce maximal synchronized spiking activity in response to synthetic mixtures of the two components centering around the natural ratio, suggesting that behaviorally effective mixture ratios are encoded by synchronous neuronal activity. We investigated the physiological activity and morphology of downstream protocerebral neurons that responded to antennal stimulation with single pheromone components and their mixtures at various concentration ratios. Among the tested neurons, only a few gave stronger responses to the mixture at the natural ratio whereas most did not distinguish among the mixtures that were tested. We also found that the population response distinguished among the two pheromone components and their mixtures, prior to the peak population response. This observation is consistent with our previous finding that synchronous firing of antennal-lobe projection neurons reaches its maximum before the firing rate reaches its peak. Moreover, the response patterns of protocerebral neurons are diverse, suggesting that the representation of olfactory stimuli at the level of protocerebrum is complex.

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“…Rein et al (2013) present new results on octopaminergic modulatory influences at the level of AL glomeruli using calcium imaging of glomerular activation patterns in honeybees. The importance of temporal aspects in coding behaviorally relevant odorant mixtures is demonstrated by Martin et al (2013) using multi-unit electrophysiological recordings of AL neurons and behaviorally relevant mixtures of sex-pheromone components in Manudca sexta. The contribution by Rössler and Brill (2013) focuses on neurophysiological, anatomical and evolutionary aspects of parallel processing of olfactory information along the olfactory pathway, in particular using simultaneous multi-unit recordings from two sets of AL projection neurons within a dual olfactory pathway in the honeybee .…”

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confidence: 99%