Pheromone Detection by a Pheromone Emitter: A Small Sex Pheromone-Specific Processing System in the Female American Cockroach

Nishino, Hiroshi; Iwasaki, Mio; Mizunami, Makoto

doi:10.1093/chemse/bjq122

Cited by 17 publications

(25 citation statements)

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“…Type2 and type1 PNs had dendrites in the antero-dorsal and postero-ventral group glomeruli, respectively ( Figures 1E,F ). Among the 106 glomeruli analyzed, only 10 postero-ventral group glomeruli were connected with the ALT-2 or ALT-3 PNs previously identified (Malun et al, 1993), and two macroglomeruli were connected with sex pheromone-sensitive PNs that terminated in specific regions of higher brain centers (Nishino et al, 2011, 2012a). Here, we focused on the two major streams formed by type1 and type2 PNs.…”

Section: Resultsmentioning

confidence: 95%

“…Retrograde staining of PNs revealed all glomeruli were innervated by PNs running m-ALT and nearby tracts in the cockroach ( Figures 1A,B ). Except for two sex pheromone-receptive macroglomeruli that were each innervated by multiple PNs (Nishino et al, 2011), individual ordinary glomeruli were in principle innervated by a single uniglomerular PN ( Figures 1A,B ; Ernst and Boeckh, 1983). PNs innervating the antero-dorsal group glomeruli (arrowheads in Figures 1A,B ), and those innervating the postero-ventral group glomeruli (arrows in Figure 1B ) formed two distinct axon bundles in the AL.…”

Section: Resultsmentioning

confidence: 99%

“…The method used for intracellular recording and staining from individual PNs of the cockroach was modified from methods reported in our previous studies (Nishino et al, 2003, 2011, 2012a; Watanabe et al, 2012a). Cockroaches were briefly anesthetized and mounted on experimental chambers with low-melting point wax.…”

Section: Methodsmentioning

confidence: 99%

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Two Parallel Olfactory Pathways for Processing General Odors in a Cockroach

Watanabe

Nishino

Mizunami

et al. 2017

Front. Neural Circuits

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In animals, sensory processing via parallel pathways, including the olfactory system, is a common design. However, the mechanisms that parallel pathways use to encode highly complex and dynamic odor signals remain unclear. In the current study, we examined the anatomical and physiological features of parallel olfactory pathways in an evolutionally basal insect, the cockroach Periplaneta americana. In this insect, the entire system for processing general odors, from olfactory sensory neurons to higher brain centers, is anatomically segregated into two parallel pathways. Two separate populations of secondary olfactory neurons, type1 and type2 projection neurons (PNs), with dendrites in distinct glomerular groups relay olfactory signals to segregated areas of higher brain centers. We conducted intracellular recordings, revealing olfactory properties and temporal patterns of both types of PNs. Generally, type1 PNs exhibit higher odor-specificities to nine tested odorants than type2 PNs. Cluster analyses revealed that odor-evoked responses were temporally complex and varied in type1 PNs, while type2 PNs exhibited phasic on-responses with either early or late latencies to an effective odor. The late responses are 30–40 ms later than the early responses. Simultaneous intracellular recordings from two different PNs revealed that a given odor activated both types of PNs with different temporal patterns, and latencies of early and late responses in type2 PNs might be precisely controlled. Our results suggest that the cockroach is equipped with two anatomically and physiologically segregated parallel olfactory pathways, which might employ different neural strategies to encode odor information.

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Section: Resultsmentioning

confidence: 95%

Section: Resultsmentioning

confidence: 99%

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Two Parallel Olfactory Pathways for Processing General Odors in a Cockroach

Watanabe

Nishino

Mizunami

et al. 2017

Front. Neural Circuits

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“…The methods used for intracellular recording from, and staining of, individual secondary olfactory interneurons of the cockroach were modified from those reported in previous studies (Nishino et al, 2003, 2011, 2012). After the brain sheath had been slightly softened by Actinase E (Kaken Seiyaku, Tokyo, Japan), the brain and platinum ground electrode were immersed in a cockroach saline solution used for intracellular recording (Yamasaki and Narahashi, 1959; NaCl 210.2 mM, KCl 3.1 mM, CaCl 2 1.8 mM, NaH 2 PO 4 0.2 mM, Na 2 HPO 4 1.8 mM, pH 7.2).…”

Section: Methodsmentioning

confidence: 99%

Spatio-temporal activity patterns of odor-induced synchronized potentials revealed by voltage-sensitive dye imaging and intracellular recording in the antennal lobe of the cockroach

Watanabe¹,

Ai²,

Yokohari³

2012

Front. Syst. Neurosci.

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In animals, odor qualities are represented as both spatial activity patterns of glomeruli and temporal patterns of synchronized oscillatory signals in the primary olfactory centers. By optical imaging of a voltage-sensitive dye (VSD) and intracellular recording from secondary olfactory interneurons, we examined possible neural correlates of the spatial and temporal odor representations in the primary olfactory center, the antennal lobe (AL), of the cockroach Periplaneta americana. Voltage-sensitive dye imaging revealed that all used odorants induced odor-specific temporal patterns of depolarizing potentials in specific combinations of anterior glomeruli of the AL. The depolarizing potentials evoked by different odorants were temporally synchronized across glomeruli and were termed “synchronized potentials.” These observations suggest that odor qualities are represented by spatio-temporal activity patterns of the synchronized potentials across glomeruli. We also performed intracellular recordings and stainings from secondary olfactory interneurons, namely projection neurons and local interneurons. We analyzed the temporal structures of enanthic acid-induced action potentials of secondary olfactory interneurons using simultaneous paired intracellular recording from two given neurons. Our results indicated that the multiple local interneurons synchronously fired in response to the olfactory stimulus. In addition, all stained enanthic acid-responsive projection neurons exhibited dendritic arborizations within the glomeruli where the synchronized potentials were evoked. Since multiple local interneurons are known to synapse to a projection neuron in each glomerulus in the cockroach AL, converging inputs from local interneurons to the projection neurons appear to contribute the odorant specific spatio-temporal activity patterns of the synchronized potentials.

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“…Ablation of the largest chemosensory organs, antennae, resulted in a delay in ootheca production compared to that in intact females, although complete ablation of the antennae may have side-effects related to loss of sensory input [34]. Unexpectedly, a typical female-specific odor, the primary sex pheromone component (periplanone-B), did not promote ootheca production, despite the fact that the female P. americana is equipped with a specific olfactory glomerulus in its first-order olfactory center that processes periplanone-B [35, 36]. …”

Section: Discussionmentioning

confidence: 99%

Group-housed females promote production of asexual ootheca in American cockroaches

Iwasaki

Hosono

et al. 2017

Zoological Lett

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BackgroundFacultative parthenogenesis, seen in many animal phyla, is a reproductive strategy in which females are able to generate offspring when mating partners are unavailable. In some subsocial and eusocial insects, parthenogenesis is often more prevalent than sexual reproduction. However, little is known about how social cooperation is linked to the promotion of parthenogenesis. The domiciliary cockroach Periplaneta americana is well-suited to addressing this issue as this species belongs to the superfamily Blattoidea, which diverged into eusocial termites and shows facultative parthenogenesis.ResultsWe studied environmental factors that influence asexual production of ootheca using behavioral assays in P. americana. When more than three virgin females immediately after the imaginal molt were kept together in a small sealed container, they tended to produce egg cases (oothecae) via parthenogenesis earlier than did isolated females, resulting in apparent synchronization of ootheca production, even among females housed in different containers. In contrast, virgin females housed with genitalia-ablated males or group-housed females with antennae ablated did not significantly promote ootheca production compared to isolated females. Daily addition of the primary sex pheromone component to the container did not promote ootheca production in isolated females. Another line of study showed that grouped females make parthenogenesis more sustainable than previously known; a founder colony of 15 virgin females was sufficient to produce female progeny for a period of more than three years.ConclusionsGroup-housed females promote and stabilize asexual ootheca production compared to isolated females, and that this promotion is triggered by female-specific chemosensory signals (other than sex pheromone) primarily detected by antennae. Promotion of ootheca production between females is likely to be an early stage of social cooperation, reminiscent of the foundation and maintenance of a colony by female pairs in the eusocial termite Reticulitermes speratus.Electronic supplementary materialThe online version of this article (doi:10.1186/s40851-017-0063-x) contains supplementary material, which is available to authorized users.

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Pheromone Detection by a Pheromone Emitter: A Small Sex Pheromone-Specific Processing System in the Female American Cockroach

Cited by 17 publications

References 43 publications

Two Parallel Olfactory Pathways for Processing General Odors in a Cockroach

Two Parallel Olfactory Pathways for Processing General Odors in a Cockroach

Spatio-temporal activity patterns of odor-induced synchronized potentials revealed by voltage-sensitive dye imaging and intracellular recording in the antennal lobe of the cockroach

Group-housed females promote production of asexual ootheca in American cockroaches

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