Influence of receptor axons on the formation of olfactory glomeruli in a hemimetabolous insect, the cockroachPeriplaneta americana

Salecker, Iris; Boeckh, Jürgen

doi:10.1002/(sici)1096-9861(19960624)370:2<262::aid-cne9>3.0.co;2-0

Cited by 24 publications

(3 citation statements)

References 78 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…To address this question, we developed an optical imaging technique using a voltage-sensitive dye (VSD) in the AL of the cockroach, Periplaneta americana . In the cockroach AL, 205 unambiguously identified glomeruli are divided into two major groups: the antero-dorsal and the postero-ventral groups (Salecker and Boeckh, 1996; Nishino and Mizunami, 2006; Watanabe et al, 2010, 2012; Nishino et al, 2012). The antero-dorsal group consists of small oval-shaped glomeruli that receive sensory inputs from antennal perforated basiconic sensilla, whereas the postero-ventral group is composed of variously-shaped large glomeruli receiving sensory inputs from trichoid and grooved basiconic sensilla of the antenna (Nishino and Mizunami, 2006; Watanabe et al, 2010, 2012).…”

Section: Introductionmentioning

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.

View full text Add to dashboard Cite

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.

show abstract

Section: Introductionmentioning

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.

View full text Add to dashboard Cite

show abstract

“…The olfactory circuit of P. americana has been extensively investigated thanks to its robustness and accessibility for longterm electrophysiology and neuronal tracing (Ernst and Boeckh, 1983;Hösl, 1990;Husch et al, 2009;Malun et al, 1993;Salecker and Boeckh, 1996). Hence, being amongst the best-described olfactory systems, it provides an excellent model for investigating how a hemimetabolous insect encodes odorants.…”

Section: Discussionmentioning

confidence: 99%

Coding of odour and space in the hemimetabolous insect Periplaneta americana

Paoli

Nishino

Couzin-Fuchs

et al. 2020

Journal of Experimental Biology

View full text Add to dashboard Cite

The general architecture of the olfactory system is highly conserved from insects to humans, but neuroanatomical and physiological differences can be observed across species. The American cockroach, inhabiting dark shelters with a rather stable olfactory landscape, is equipped with long antennae used for sampling the surrounding airspace for orientation and navigation. The antennae's exceptional length provides a wide spatial working range for odour detection; however, it is still largely unknown whether and how this is also used for mapping the structure of the olfactory environment. By selectively labelling antennal lobe projection neurons with a calciumsensitive dye, we investigated the logic of olfactory coding in this hemimetabolous insect. We show that odour responses are stimulus specific and concentration dependent, and that structurally related odorants evoke physiologically similar responses. By using spatially confined stimuli, we show that proximal stimulations induce stronger and faster responses than distal ones. Spatially confined stimuli of the female pheromone periplanone B activate a subregion of the male macroglomerulus. Thus, we report that the combinatorial logic of odour coding deduced from holometabolous insects applies also to this hemimetabolous species. Furthermore, a fast decrease in sensitivity along the antenna, not supported by a proportionate decrease in sensillar density, suggests a neural architecture that strongly emphasizes neuronal inputs from the proximal portion of the antenna.

show abstract

“…The olfactory circuit of P. americana has been extensively investigated thanks to its robustness and accessibility for long-term electrophysiology and neuronal tracing (Ernst and Boeckh, 1983; Hösl, 1990; Husch et al, 2009; Malun et al, 1993; Salecker and Boeckh, 1996). Hence, being amongst the best described olfactory systems, it provides an excellent model for understanding which olfactory coding rules apply to hemimetabolous insects.…”

Section: Discussionmentioning

confidence: 99%

Coding of odour and space in the hemimetabolous insect Periplaneta americana

Paoli

Nishino

Couzin-Fuchs

et al. 2019

Preprint

View full text Add to dashboard Cite

statementBy selective labelling the cockroach's antennal lobe output neurons, we investigated the logic of olfactory coding in a hemimetabolous insect, showing that odour responses are stimulus-specific, concentration-dependent, and preserve information on the spatial structure of the stimulus. AbstractThe general architecture of the olfactory system is highly conserved from insects to humans, but neuroanatomical and physiological differences can be observed across species. The American cockroach, inhabiting dark shelters with a rather stable olfactory landscape, is equipped with long antennae used for sampling the surrounding air-space for orientation and navigation. The antennae's exceptional length provides a wide spatial working range for odour detection; however, it is still largely unknown whether and how this is also used for mapping the structure of the olfactory environment. By selective labelling antennal lobe projection neurons with a calcium sensitive dye, we investigated the logic of olfactory coding in this hemimetabolous insect. We show that odour responses are stimulus-specific and concentration-dependent, and that structurally related odorants evoke physiologically similar responses. By using spatially confined stimuli, we show that proximal stimulations induce stronger and faster responses than distal ones. Spatially confined stimuli of the female pheromone periplanone-B activate sub-region of the male macroglomerulus. Thus, we report that the combinatorial logic of odour coding deduced from holometabolous insects applies also to this hemimetabolous species. Furthermore, a fast decrease in sensitivity along the antenna, not supported by a proportionate decrease in sensillar density, suggests a neural architecture that strongly emphasizes neuronal inputs from the proximal portion of the antenna. 1983; Schaller, 1978; Watanabe et al., 2012). Their axons innervate two exceptionally large glomeruli, which form the macroglomerular complex (Schaller, 1978; Watanabe et al., 2012).Glomeruli are interconnected by a dense network of local interneurons (Fusca et al., 2013; Husch et al., 2009), and processed olfactory information is relayed to higher order brain centres by uniglomerular (uPNs) and multiglomerular projection neurons (mPNs) (Malun et al., 1993).Uniglomerular PNs extend their dendritic arborization in a single glomerulus, thus receiving direct input from only one OSN type. Two subgroups of uPNs innervate distinct glomerular populations, their cell bodies clustering in two distinct groups in the antero-dorsal side of the AL (Strausfeld and Li, 1999; Watanabe et al., 2017). In the American cockroach, each ordinary glomerulus is innervated by only one uPN, whereas the macroglomerulus (MG) is innervated by multiple uPNs with a highly stereotyped topology (Galizia, 2018; Nishino et al., 2018). Two main PN axon bundles exit from the medio-dorsal side of the antennal lobe (note that all orientations here provided are in body axis system), and relay odour-related information to the protocerebrum. ...

show abstract

Influence of receptor axons on the formation of olfactory glomeruli in a hemimetabolous insect, the cockroachPeriplaneta americana

Cited by 24 publications

References 78 publications

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

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

Coding of odour and space in the hemimetabolous insect Periplaneta americana

Coding of odour and space in the hemimetabolous insect Periplaneta americana

Contact Info

Product

Resources

About