Publications by authors named "Bente G Berg"

25 Publications

  • Page 1 of 1

Neuronal architecture and functional mapping of the taste center of larval Helicoverpa armigera (Lepidoptera: Noctuidae).

Insect Sci 2021 Aug 24. Epub 2021 Aug 24.

Department of Entomology, College of Plant Protection, Henan Agricultural University, Zhengzhou, 450002, China.

The sense of taste plays a crucial role in herbivorous insects by discriminating nutrients from complex plant metabolic compounds. The peripheral coding of taste has been thoroughly studied in many insect species, but the central gustatory pathways are poorly described. In the present study, we characterized single neurons in the gnathal ganglion of Helicoverpa armigera larvae using the intracellular recording/staining technique. We identified different types of neurons, including sensory neurons, interneurons, and motor neurons. The morphologies of these neurons were largely diverse and their arborizations seemingly covered the whole gnathal ganglion. The representation of the single neurons responding to the relevant stimuli of sweet and bitter cues showed no distinct patterns in the gnathal ganglion. We postulate that taste signals may be processed in a manner consistent with the principle of population coding in the gnathal ganglion of H. armigera larvae. This article is protected by copyright. All rights reserved.
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http://dx.doi.org/10.1111/1744-7917.12965DOI Listing
August 2021

A unified platform to manage, share, and archive morphological and functional data in insect neuroscience.

Elife 2021 08 24;10. Epub 2021 Aug 24.

Department of Biology, Lund University, Lund, Sweden.

Insect neuroscience generates vast amounts of highly diverse data, of which only a small fraction are findable, accessible and reusable. To promote an open data culture, we have therefore developed the InsectBrainDatabase (), a free online platform for insect neuroanatomical and functional data. The facilitates biological insight by enabling effective cross-species comparisons, by linking neural structure with function, and by serving as general information hub for insect neuroscience. The allows users to not only effectively locate and visualize data, but to make them widely available for easy, automated reuse via an application programming interface. A unique private mode of the database expands the functionality beyond public data deposition, additionally providing the means for managing, visualizing, and sharing of unpublished data. This dual function creates an incentive for data contribution early in data management workflows and eliminates the additional effort normally associated with publicly depositing research data.
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http://dx.doi.org/10.7554/eLife.65376DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8457822PMC
August 2021

Antennal-lobe neurons in the moth Helicoverpa armigera: Morphological features of projection neurons, local interneurons, and centrifugal neurons.

J Comp Neurol 2021 05 5;529(7):1516-1540. Epub 2020 Oct 5.

Chemosensory lab, Department of Psychology, Norwegian University of Science and Technology, Trondheim, Norway.

The relatively large primary olfactory center of the insect brain, the antennal lobe (AL), contains several heterogeneous neuronal types. These include projection neurons (PNs), providing olfactory information to higher-order neuropils via parallel pathways, and local interneurons (LNs), which provide lateral processing within the AL. In addition, various types of centrifugal neurons (CNs) offer top-down modulation onto the other AL neurons. By performing iontophoretic intracellular staining, we collected a large number of AL neurons in the moth, Helicoverpa armigera, to examine the distinct morphological features of PNs, LNs, and CNs. We characterize 190 AL neurons. These were allocated to 25 distinct neuronal types or sub-types, which were reconstructed and placed into a reference brain. In addition to six PN types comprising 15 sub-types, three LN and seven CN types were identified. High-resolution confocal images allowed us to analyze AL innervations of the various reported neurons, which demonstrated that all PNs innervating ventroposterior glomeruli contact a protocerebral neuropil rarely targeted by other PNs, that is the posteriorlateral protocerebrum. We also discuss the functional roles of the distinct CNs, which included several previously uncharacterized types, likely involved in computations spanning from multisensory processing to olfactory feedback signalization into the AL.
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http://dx.doi.org/10.1002/cne.25034DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8048870PMC
May 2021

A Novel Major Output Target for Pheromone-Sensitive Projection Neurons in Male Moths.

Front Cell Neurosci 2020 8;14:147. Epub 2020 Jun 8.

Chemosensory Laboratory, Department of Psychology, Norwegian University of Science and Technology, Trondheim, Norway.

Even though insects have comparably small brains, they achieve astoundingly complex behaviors. One example is flying moths tracking minute amounts of pheromones using olfactory circuits. The tracking distance can be up to 1 km, which makes it essential that male moths respond efficiently and reliably to very few pheromone molecules. The male-specific macroglomerular complex (MGC) in the moth antennal lobe contains circuitry dedicated to pheromone processing. Output neurons from this region project along three parallel pathways, the medial, mediolateral, and lateral tracts. The MGC-neurons of the lateral tract are least described and their functional significance is mainly unknown. We used mass staining, calcium imaging, and intracellular recording/staining to characterize the morphological and physiological properties of these neurons in the noctuid moth, . All lateral-tract MGC neurons targeted the column, a small region within the superior intermediate neuropil. We identified this region as a unique converging site for MGC lateral-tract neurons responsive to pheromones, as well as a dense congregating site for plant odor information since a substantial number of lateral-tract neurons from ordinary glomeruli (OG) also terminates in this region. The lateral-tract MGC-neurons responded with a shorter peak latency than the well-described neurons in the medial tract. Different from the medial-tract MGC neurons encoding odor quality important for species-specific signal identification, those in the lateral tract convey a more robust and rapid signal-potentially important for fast control of hard-wired behavior.
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http://dx.doi.org/10.3389/fncel.2020.00147DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7294775PMC
June 2020

Brain Organization of : A Hemipteran Species With Prominent Antennal Lobes.

Front Neuroanat 2019 17;13:70. Epub 2019 Jul 17.

Department of Entomology, College of Plant Protection, Henan Agricultural University, Zhengzhou, China.

The anatomical organization of distinct regions in the insect brain often reflects their functions. In the present study, the brain structure of was examined by using immunolabeling and three-dimensional reconstruction. The results revealed the location and volume of prominent neuropils, such as the antennal lobes (AL), optic lobes (OL), anterior optic tubercles (AOTU), central body (CB), lateral accessory lobes (LAL), mushroom lobes, and distinct tritocerebral neuropils. As expected, this brain is similar to that of other insects. One exception, however, is that the antennal lobes were found to be the most prominent neuropils. Their size relative to the entire brain is the largest among all insect species studied so far. In contrast, the calyx, a region getting direct input from the antennal lobe, has a smaller size relative to the brain than that of other species. These findings may suggest that olfaction plays an essential role for .
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http://dx.doi.org/10.3389/fnana.2019.00070DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6654032PMC
July 2019

Central Projections of Antennal and Labial Palp Sensory Neurons in the Migratory Armyworm .

Front Cell Neurosci 2017 21;11:370. Epub 2017 Nov 21.

State Key Laboratory for Biology of Plant Disease and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China.

The oriental armyworm, (Walker), is a polyphagous, migratory pest relying on olfactory cues to find mates, locate nectar, and guide long-distance flight behavior. In the present study, a combination of neuroanatomical techniques were utilized on this species, including backfills, confocal microscopy, and three-dimensional reconstructions, to trace the central projections of sensory neurons from the antenna and the labial pit organ, respectively. As previously shown, the axons of the labial sensory neurons project via the ipsilateral labial nerve and terminate in three main areas of the central nervous system: (1) the labial-palp pit organ glomerulus of each antennal lobe, (2) the gnathal ganglion, and (3) the prothoracic ganglion of the ventral nerve cord. Similarly, the antennal sensory axons project to multiple areas of the central nervous system. The ipsilateral antennal nerve targets mainly the antennal lobe, the antennal mechanosensory and motor center, and the prothoracic and mesothoracic ganglia. Specific staining experiments including dye application to each of the three antennal segments indicate that the antennal lobe receives input from flagellar olfactory neurons exclusively, while the antennal mechanosensory and motor center is innervated by mechanosensory neurons from the whole antenna, comprising the flagellum, pedicle, and scape. The terminals in the mechanosensory and motor center are organized in segregated zones relating to the origin of neurons. The flagellar mechanosensory axons target anterior zones, while the pedicular and scapal axons terminate in posterior zones. In the ventral nerve cord, the processes from the antennal sensory neurons terminate in the motor area of the thoracic ganglia, suggesting a close connection with motor neurons. Taken together, the numerous neuropils innervated by axons both from the antenna and labial palp indicate the multiple roles these sensory organs serve in insect behavior.
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http://dx.doi.org/10.3389/fncel.2017.00370DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5702295PMC
November 2017

Distribution of tachykinin-related peptides in the brain of the tobacco budworm Heliothis virescens.

J Comp Neurol 2017 Dec 15;525(18):3918-3934. Epub 2017 Sep 15.

Department of Biology, Animal Physiology, Philipps University, Marburg, 35032, Germany.

Invertebrate tachykinin-related peptides (TKRPs) comprise a group of signaling molecules having sequence similarities to mammalian tachykinins. A growing body of evidence has demonstrated the presence of TKRPs in the central nervous system of insects. In this investigation, we used an antiserum against locustatachykinin-II to reveal the distribution pattern of these peptides in the brain of the moth Heliothis virescens. Immunolabeling was found throughout the brain of the heliothine moth. Most of the roughly 500 locustatachykinin-II immunoreactive cell bodies, that is, ca. 400, were located in the protocerebrum, whereas the rest was distributed in the deutocerebrum, tritocerebrum, and the gnathal ganglion. Abundant immunoreactive processes were located in the same regions. Labeled processes in the protocerebrum were especially localized in optic lobe, central body, lateral accessory lobe, superior protocerebrum, and lateral protocerebrum, while those in the deutocerebrum were present exclusively in the antennal lobe. In addition to brain interneurons, four pairs of median neurosecretory cells in the pars intercerebralis with terminal processes in the corpora cardiaca and aorta wall were immunostained. No sexual dimorphism in immunoreactivity was found. Comparing the data obtained here with findings from other insect species reveals considerable differences, suggesting species-specific roles of tachykinin-related peptides in insects.
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http://dx.doi.org/10.1002/cne.24310DOI Listing
December 2017

Coincidence of pheromone and plant odor leads to sensory plasticity in the heliothine olfactory system.

PLoS One 2017 3;12(5):e0175513. Epub 2017 May 3.

Norwegian University of Science and Technology (NTNU), Department of Psychology, Trondheim, Norway.

Male moths possess a highly specialized olfactory system comprised of two segregated sub-arrangements dedicated to processing information about plant odors and pheromones, respectively. Communication between these two sub-systems has been described at the peripheral level, but relatively little is known about putative interactions at subsequent synaptic relays. The male moth faces the challenge of seeking out the conspecific female in a highly dynamic odor world. The female-produced pheromone blend, which is a limited resource serving as guidance for the male, will reach his antennae in intermittent pockets of odor filaments mixed with volatiles from various plants. In the present study we performed calcium imaging for measuring odor-evoked responses in the uni-glomerular antennal-lobe projection neurons (analog to mitral cells in the vertebrate olfactory bulb) of Helicoverpa armigera. In order to investigate putative interactions between the two sub-systems tuned to plant volatiles and pheromones, respectively, we performed repeated stimulations with a selection of biologically relevant odors. We found that paired stimulation with a plant odor and the pheromone led to suppressed responses in both sub-systems as compared to those evoked during initial stimulation including application of each odor stimulus alone. The fact that the suppression persisted also after pairing, indicates the existence of a Hebbian-like plasticity in the primary olfactory center established by temporal pairing of the two odor stimulation categories.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0175513PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5414983PMC
September 2017

Individual Neurons Confined to Distinct Antennal-Lobe Tracts in the Heliothine Moth: Morphological Characteristics and Global Projection Patterns.

Front Neuroanat 2016 24;10:101. Epub 2016 Oct 24.

Department of Psychology, Norwegian University of Science and Technology Trondheim, Norway.

To explore fundamental principles characterizing chemosensory information processing, we have identified antennal-lobe projection neurons in the heliothine moth, including several neuron types not previously described. Generally, odor information is conveyed from the primary olfactory center of the moth brain, the antennal lobe, to higher brain centers via projection neuron axons passing along several parallel pathways, of which the medial, mediolateral, and lateral antennal-lobe tract are considered the classical ones. Recent data have revealed the projections of the individual tracts more in detail demonstrating three main target regions in the protocerebrum; the calyces are innervated mainly by the medial tract, the superior intermediate protocerebrum by the lateral tract exclusively, and the lateral horn by all tracts. In the present study, we have identified, via iontophoretic intracellular staining combined with confocal microscopy, individual projection neurons confined to the tracts mentioned above, plus two additional ones. Further, using the visualization software AMIRA, we reconstructed the stained neurons and registered the models into a standard brain atlas, which allowed us to compare the termination areas of individual projection neurons both across and within distinct tracts. The data demonstrate a morphological diversity of the projection neurons within distinct tracts. Comparison of the output areas of the neurons confined to the three main tracts in the lateral horn showed overlapping terminal regions for the medial and mediolateral tracts; the lateral tract neurons, on the contrary, targeted mostly other output areas in the protocerebrum.
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http://dx.doi.org/10.3389/fnana.2016.00101DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5075568PMC
October 2016

A global-wide search for sexual dimorphism of glomeruli in the antennal lobe of female and male Helicoverpa armigera.

Sci Rep 2016 10 11;6:35204. Epub 2016 Oct 11.

Department of Entomology, College of Plant Protection, Henan Agricultural University, Zhengzhou, 450002, China.

By using immunostaining and three-dimensional reconstruction, the anatomical organization of the antennal lobe glomeruli of the female cotton bollworm Helicoverpa armigera was investigated. Eighty-one glomeruli were identified, 15 of which were not previously discovered. The general anatomical organization of the AL of female is similar to that of male and all glomeruli were classified into four sub-groups, including the female-specific glomerular complex, posterior complex, labial-palp pit organ glomerulus, and ordinary glomeruli. A global-wide comparison on the complete glomerular map of female and male was performed and for the first time the quantitative difference in volume for each individual homologous glomerulus was analyzed. We found that the sexual dimorphism includes not only the sex-specific glomeruli but also some of the other glomeruli. The findings in the present study may provide a reference to examine the antennal-lobe organization more in detail and to identify new glomeruli in other moth species. In addition, the complete identification and global-wide comparison of the sexes provide an important basis for mapping the function of distinct glomeruli and for understanding neural mechanisms underlying sexually dimorphic olfactory behaviors.
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http://dx.doi.org/10.1038/srep35204DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5057091PMC
October 2016

Glomerular identification in the antennal lobe of the male moth Helicoverpa armigera.

J Comp Neurol 2016 10 3;524(15):2993-3013. Epub 2016 May 3.

Department of Psychology, Norwegian University of Science and Technology, Trondheim, 7489, Norway.

This study investigates anatomical organization of the antennal lobe (AL) glomeruli of the male cotton bollworm Helicoverpa armigera by synaptic antibody staining combined with three-dimensional reconstruction. To identify all glomeruli, their boundaries were accurately determined by means of several additional staining techniques visualizing the neuron categories forming the characteristic spherical neuropils. In total, 78-80 glomeruli were identified in the male H. armigera. The number of glomeruli was considerably larger than that previously reported in this species. Thus, compared with previous studies, we identified 15 new glomeruli, G63-G77. Most of them are located in the posterior part of the AL, which was previously considered to be a part of the protocerebrum. From the general anatomical organization of the AL glomeruli of H. armigera, we classified these neuropil structures into four groups, the macroglomerular complex, posterior complex, labial-palp pit organ glomerulus, and ordinary glomeruli. The complete identification of glomeruli is important for future studies seeking to explore further the coding mechanisms residing within the primary olfactory center of the moth brain. J. Comp. Neurol. 524:2993-3013, 2016. © 2016 Wiley Periodicals, Inc.
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http://dx.doi.org/10.1002/cne.24003DOI Listing
October 2016

Representation of pheromones, interspecific signals, and plant odors in higher olfactory centers; mapping physiologically identified antennal-lobe projection neurons in the male heliothine moth.

Front Syst Neurosci 2014 9;8:186. Epub 2014 Oct 9.

Department of Psychology, Norwegian University of Science and Technology (NTNU) Trondheim, Norway.

The arrangement of anatomically separated systems for information about general and pheromone odorants is well documented at the initial levels of the olfactory pathway both in vertebrates and insects. In the primary olfactory center of the moth brain, for example, a few enlarged glomeruli situated dorsally, at the entrance of the antennal nerve, are devoted to information about female-produced substances whereas a set of more numerous ordinary glomeruli (OG) receives input about general odorants. Heliothine moths are particularly suitable for studying central chemosensory mechanisms not only because of their anatomically separated systems for plant odors and pheromones but also due to their use of female-produced substances in communication across the species. Thus, the male-specific system of heliothine moths includes two sub-arrangements, one ensuring attraction and mating behavior by carrying information about pheromones released by conspecifics, and the other inhibition of attraction via signal information emitted from heterospecifics. Based on previous tracing experiments, a general chemotopic organization of the male-specific glomeruli has been demonstrated in a number of heliothine species. As compared to the well explored organization of the moth antennal lobe (AL), demonstrating a non-overlapping representation of the biologically relevant stimuli, less is known about the neural arrangement residing at the following synaptic level, i.e., the mushroom body calyces and the lateral horn. In the study presented here, we have labeled physiologically characterized antennal-lobe projection neurons in males of the two heliothine species, Heliothis virescens and Helicoverpa assulta, for the purpose of mapping their target regions in the protocerebrum. In order to compare the representation of plant odors, pheromones, and interspecific signals in the higher brain regions of each species, we have created standard brain atlases and registered three-dimensional models of distinct uniglomerular projection neuron types into the relevant atlas.
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http://dx.doi.org/10.3389/fnsys.2014.00186DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4191081PMC
October 2014

Central projections of gustatory receptor neurons in the medial and the lateral sensilla styloconica of Helicoverpa armigera larvae.

PLoS One 2014 16;9(4):e95401. Epub 2014 Apr 16.

Department of Entomology, College of Plant Protection, Henan Agricultural University, Zhengzhou, Henan, China.

Food selection behavior of lepidopteran larvae is predominantly governed by the activation of taste neurons present in two sensilla styloconica located on the galea of the maxilla. In this study, we present the ultrastructure of the sensilla styloconica and the central projection pattern of their associated receptor neurons in larvae of the heliothine moth, Helicoverpa armigera. By means of light microscopy and scanning electron microscopy, the previous findings of two morphologically fairly similar sensilla comprising a socketed conic tip inserted into a large peg were confirmed. However, the peg size of the medial sensillum was found to be significantly bigger than that of the lateral sensillum. The sensory neurons derived from each sensillum styloconicum were mapped separately using anterograde staining experiments combined with confocal laser-scanning microscopy. For determining the afferents' target regions relative to each other, we reconstructed the labeled axons and placed them into a common reference framework. The sensory axons from both sensilla projected via the ipsilateral maxillary nerve to the suboesophageal ganglion and further through the ipsilateral circumoesophageal connective to the brain. In the suboesophageal ganglion, the sensory projections targeted two areas of the ipsilateral maxillary neuropil, one located in the ventrolateral neuromere and the other adjacent to the neuromere midline. In the brain, the axon terminals targeted the dorso-anterior area of the ipsilateral tritocerebrum. As confirmed by the three-dimensional reconstructions, the target regions of the neural projections originating from each of the two sensilla styloconica were identical.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0095401PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3989337PMC
June 2015

Tracing and 3-dimensional representation of the primary afferents from the moth ear.

Arthropod Struct Dev 2014 May 13;43(3):231-41. Epub 2014 Apr 13.

Norwegian University of Science and Technology, Department of Psychology, Neuroscience Unit, 7491 Trondheim, Norway. Electronic address:

Heliothine moths perceive acoustic information via two auditory sensory neurons only. Previous cobalt staining experiments have described the projection pattern of the two auditory neurons, called the A1 and the A2 cell, plus one additional neuron, the so-called B cell, up to the prothorax. We have obtained new and improved data about the projection pattern of the three sensory afferents by means of fluorescent staining experiments combined with scanning confocal microscopy. The present data show the fine structure of each sensory axon that arises from the moth ear and its ascending pathway relative to that of the others. In accordance with the previous data, the A2 auditory cell was found to extend projections in the pterothorax only. A novel finding is that terminal branches of the A2 cell cross the midline. The staining pattern of the two remaining neurons, the A1 and B cell, which project tightly together in the thoracic ganglia, differ somewhat from that previously described. As demonstrated here, one of these two neurons, the A1 cell, terminates in the prothoracic ganglion whereas the other, the B cell, projects further on via the cervical connectives to the subesophageal ganglion. The current data, therefore, indicate that none of the auditory afferents in the heliothine moth projects to the brain.
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http://dx.doi.org/10.1016/j.asd.2014.04.001DOI Listing
May 2014

Processing of Pheromone Information in Related Species of Heliothine Moths.

Insects 2014 Oct 14;5(4):742-61. Epub 2014 Oct 14.

State Key Laboratory for Biology of Plant Disease and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China.

In heliothine moths, the male-specific olfactory system is activated by a few odor molecules, each of which is associated with an easily identifiable glomerulus in the primary olfactory center of the brain. This arrangement is linked to two well-defined behavioral responses, one ensuring attraction and mating behavior by carrying information about pheromones released by conspecific females and the other inhibition of attraction via signal information emitted from heterospecifics. The chance of comparing the characteristic properties of pheromone receptor proteins, male-specific sensory neurons and macroglomerular complex (MGC)-units in closely-related species is especially intriguing. Here, we review studies on the male-specific olfactory system of heliothine moths with particular emphasis on five closely related species, i.e., Heliothis virescens, Heliothis subflexa, Helicoverpa zea, Helicoverpa assulta and Helicoverpa armigera.
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http://dx.doi.org/10.3390/insects5040742DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4592608PMC
October 2014

Sound-sensitive neurons innervate the ventro-lateral protocerebrum of the heliothine moth brain.

Cell Tissue Res 2014 Feb 10;355(2):289-302. Epub 2013 Dec 10.

Department of Psychology/Neuroscience Unit, MTFS, Norwegian University of Science and Technology (NTNU), 7489, Trondheim, Norway,

Many noctuid moth species perceive ultrasound via tympanic ears that are located at the metathorax. Whereas the neural processing of auditory information is well studied at the peripheral and first synaptic level, little is known about the features characterizing higher order sound-sensitive neurons in the moth brain. During intracellular recordings from the lateral protocerebrum in the brain of three noctuid moth species, Heliothis virescens, Helicoverpa armigera and Helicoverpa assulta, we found an assembly of neurons responding to transient sound pulses of broad bandwidth. The majority of the auditory neurons ascended from the ventral cord and ramified densely within the anterior region of the ventro-lateral protocerebrum. The physiological and morphological characteristics of these auditory neurons were similar. We detected one additional sound-sensitive neuron, a brain interneuron with its soma positioned near the calyces of mushroom bodies and with numerous neuronal processes in the ventro-lateral protocerebrum. Mass-staining of ventral-cord neurons supported the assumption that the ventro-lateral region of the moth brain was the main target for the auditory projections ascending from the ventral cord.
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http://dx.doi.org/10.1007/s00441-013-1749-9DOI Listing
February 2014

Fine structure and primary sensory projections of sensilla located in the labial-palp pit organ of Helicoverpa armigera (Insecta).

Cell Tissue Res 2013 Sep 5;353(3):399-408. Epub 2013 Jun 5.

Department of Entomology, College of Plant Protection, Henan Agricultural University, Zhengzhou, Henan, 450002, China.

The fine structure and primary sensory projections of sensilla located in the labial-palp pit organ of the cotton bollworm Helicoverpa armigera (Insecta, Lepidoptera) are investigated by scanning electron and transmission electron microscopy combined with confocal laser scanning microscopy. The pit organ located on the third segment of the labial palp is about 300 μm deep with a 60-μm-wide opening, each structure containing about 1200 sensilla. Two sensillum types have been found, namely hair-shaped and club-shaped sensilla, located on the upper and lower half of the pit, respectively. Most sensilla possess a single dendrite. The dendrite housed by the club-shaped sensilla is often split into several branches or becomes lamellated in the outer segment. As reported previously, the sensory axons of the sensilla in the labial pit organ form a bundle entering the ipsilateral side of the subesophageal ganglion via the labial palp nerve and project to three distinct areas: the labial pit organ glomerulus in each antennal lobe, the subesophageal ganglion and the ventral nerve cord. In the antennal lobe, the labial pit organ glomerulus is innervated by sensory axons from the labial pit organ only; no antennal afferents target this unit. One neuron has been found extending fine processes into the subesophageal ganglion and innervating the labial palp via one branch passing at the base of the labial palp nerve. The soma of this assumed motor neuron is located in the ipsilateral cell body layer of the subesophageal ganglion. Our results provide valuable knowledge concerning the neural circuit encoding information about carbon dioxide and should stimulate further investigations directed at controlling pest species such as H. armigera.
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http://dx.doi.org/10.1007/s00441-013-1657-zDOI Listing
September 2013

A multisensory centrifugal neuron in the olfactory pathway of heliothine moths.

J Comp Neurol 2013 Jan;521(1):152-68

Department of Psychology, Neuroscience Unit, Norwegian University of Science and Technology, 7491 Trondheim, Norway.

We have characterized, by intracellular recording and staining, a unique type of centrifugal neuron in the brain olfactory center of two heliothine moth species; one in Heliothis virescens and one in Helicoverpa armigera. This unilateral neuron, which is not previously described in any moth, has fine processes in the dorsomedial region of the protocerebrum and extensive neuronal branches with blebby terminals in all glomeruli of the antennal lobe. Its soma is located dorsally of the central body close to the brain midline. Mass-fills of antennal-lobe connections with protocerebral regions showed that the centrifugal neuron is, in each brain hemisphere, one within a small group of neurons having their somata clustered. In both species the neuron was excited during application of non-odorant airborne signals, including transient sound pulses of broad bandwidth and air velocity changes. Additional responses to odors were recorded from the neuron in Heliothis virescens. The putative biological significance of the centrifugal antennal-lobe neuron is discussed with regard to its morphological and physiological properties. In particular, a possible role in multisensory processes underlying the moth's ability to adapt its odor-guided behaviors according to the sound of an echo-locating bat is considered.
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http://dx.doi.org/10.1002/cne.23166DOI Listing
January 2013

Characterization of three pheromone-binding proteins (PBPs) of Helicoverpa armigera (Hübner) and their binding properties.

J Insect Physiol 2012 Jul 28;58(7):941-8. Epub 2012 Apr 28.

State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China.

Three pheromone-binding proteins of Helicoverpa armigera were cloned and expressed in Escherichia coli. In order to characterize their physiological properties, ligand-binding experiments were performed using five biologically relevant substances including sex pheromones and interspecific signals. The results showed that one of the pheromone-binding proteins, HarmPBP1, binds strongly to each of the two principal pheromone components of H. armigera, (Z)-11-tetradecenal and (Z)-9-hexadecenal, but not to the interspecific signal (Z)-9-tetracecenal. The two remaining pheromone-binding proteins, HarmPBP2 and HarmPBP3, showed only weak affinities with the ligands tested. The 3-D structure of HarmPBP1 was predicted and the docking experiments indicate that the key binding site of (Z)-9-hexadecenal to HarmPBP1 includes Thr112, Lys111, and Phe119 whereas that of (Z)-11-tetradecenal includes Ser9, Trp37, Phe36, and Phe119.
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http://dx.doi.org/10.1016/j.jinsphys.2012.04.010DOI Listing
July 2012

Arrangement of output information from the 3 macroglomerular units in the heliothine moth Helicoverpa assulta: morphological and physiological features of male-specific projection neurons.

Chem Senses 2010 Jul 9;35(6):511-21. Epub 2010 May 9.

Department of Psychology and Neuroscience Unit, MTFS, Norwegian University of Science and Technology, Olav Kyrres gate 9, Trondheim, Norway.

Helicoverpa assulta is exceptional among heliothine species studied so far as concerns composition of the pheromone blend. Previous reports have accordingly pointed out distinct characteristics in the male-specific olfactory pathway of this species, peripherally by an unusual distribution of 2 sensillum categories and centrally by a particular anatomical arrangement of the male-specific glomeruli constituting the macroglomerular complex (MGC). In order to determine the physiological tuning of the 3 MGC units in this species, we have characterized male-specific antennal-lobe projection neurons morphologically and physiologically by use of the intracellular recording and staining technique combined with confocal microscopy. The results show 2 projection neuron types of equal numbers, one that responds to the primary pheromone component, cis-9-hexadecenal, and arborizes in the cumulus and one that responds to the interspecific signal, cis-9-tetradecenal, and arborizes in the dorsomedial unit. A third type responded to the secondary pheromone component, cis-11-hexadecenal, and innervated the smaller ventral unit. The results complement previous findings from tracing of physiologically identified receptor neurons and determine for the first time the functional specificity of each glomerulus in the MGC of H. assulta. The results are particularly interesting because heliothine moths are attractive objects for comparative studies addressing questions concerning divergence of male-specific olfactory characteristics related to speciation.
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http://dx.doi.org/10.1093/chemse/bjq043DOI Listing
July 2010

Gamma-aminobutyric acid immunostaining in the antennal lobe of the moth Heliothis virescens and its colocalization with neuropeptides.

Cell Tissue Res 2009 Mar 21;335(3):593-605. Epub 2009 Jan 21.

Neuroscience Unit/Department of Psychology, Norwegian University of Science and Technology, 7489 Trondheim, Norway.

The antennal lobe is the primary processing center for olfactory information in insects. To understand further the neural circuitry of this brain area, we have investigated the distribution of gamma-aminobutyric acid (GABA) and its colocalization with neuropeptides in the antennal lobe of the noctuid moth Heliothis virescens. Immunocytochemical experiments with an antiserum against GABA showed a large number of labeled somata in the antennal lobe; these somata were located exclusively in the lateral cell cluster. Stained neurites innervating all antennal-lobe glomeruli, including the male-specific macroglomerular complex, suggested a prominent role of GABA in processing olfactory information, including signals from pheromones, interspecifically acting odors, and plant odors. Fibers in two antennocerebral tracts (the middle and dorsal antennocerebral tract) exhibited prominent GABA immunoreactivity. Double-labeling experiments revealed that immunostaining for three neuropeptides, viz., A-type allatostatin, Manduca sexta allatotropin, and FMRFamide-related peptides, was largely colocalized with GABA in cell bodies of the lateral cell cluster. The general absence of peptide immunostaining in the antennocerebral tracts strongly indicated that these peptides were colocalized with GABA in local interneurons of the antennal lobe. In contrast, tachykinin-related peptides occurred in a distinct population of local antennal-lobe neurons that did not exhibit GABA immunostaining. Thus, local interneurons that were not GABAergic were present in the moth antennal lobe.
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http://dx.doi.org/10.1007/s00441-008-0744-zDOI Listing
March 2009

Distribution of neuropeptides in the primary olfactory center of the heliothine moth Heliothis virescens.

Cell Tissue Res 2007 Feb 30;327(2):385-98. Epub 2006 Sep 30.

Neuroscience Unit, Department of Psychology, Norwegian University of Science and Technology, 7489, Trondheim, Norway.

Neuropeptides are a diverse widespread class of signaling substances in the nervous system. As a basis for the analysis of peptidergic neurotransmission in the insect olfactory system, we have studied the distribution of neuropeptides in the antennal lobe of the moth Heliothis virescens. Immunocytochemical experiments with antisera recognizing A-type allatostatins (AST-As), Manduca sexta allatotropin (Mas-AT), FMRFamide-related peptides (FaRPs), and tachykinin-related peptides (TKRPs) have shown that members of all four peptide families are present in local interneurons of the antennal lobe. Whereas antisera against AST-As, Mas-AT, and FaRPs give similar staining patterns characterized by dense meshworks of processes confined to the core of all antennal-lobe glomeruli, TKRPs are present only in neurons with blebby processes distributed throughout each glomerulus. In addition to local neurons, a pair of centrifugal neurons with cell bodies in the lateral subesophageal ganglion, arborizations in the antennal lobe, and projections in the inner antenno-cerebral tracts exhibits tachykinin immunostaining. Double-label immunofluorescence has detected the co-localization of AST-As, Mas-AT, and FaRPs in certain local interneurons, whereas TKRPs occurs in a distinct population. MALDI-TOF mass spectrometry has revealed nearly 50 mass peaks in the antennal lobe. Seven of these masses (four AST-As, two N-terminally extended FLRFamides, and Mas-AT) match known moth neuropeptides. The data thus show that local interneurons of the moth antennal lobe are highly differentiated with respect to their neuropeptide content. The antennal lobe therefore represents an ideal preparation for the future analysis of peptide signaling in insect brain.
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http://dx.doi.org/10.1007/s00441-006-0318-xDOI Listing
February 2007

Consistent organization of glomeruli in the antennal lobes of related species of heliothine moths.

J Comp Neurol 2005 Oct;491(4):367-80

Neuroscience Unit, Department of Biology, Norwegian University of Science and Technology, NO-7489 Trondheim, Norway.

The glomeruli of the antennal lobes in insects reflect the organization of the olfactory system, which is important for species-specific behaviors in response to insect- and plant-produced odorants. We studied the antennal lobes of the polyphagous moth Helicoverpa armigera and the oligophagous H. assulta (Heliothinae; Lepidoptera; Noctuidae) in order to see whether there are any anatomical differences that might elucidate how information about odorants is analyzed. Three-dimensional models of the antennal lobes were made, based on synaptic antibody staining combined with confocal laser scanning microscopy. These showed 65 glomeruli in each sex of H. armigera and 66 glomeruli in females of H. assulta. Sixty-two of the glomeruli were identified in both sexes and species and were given the same numbers. The sex-specific glomeruli included three macroglomerular units in H. armigera males, as well as three and four female-specific glomeruli in H. armigera and H. assulta, respectively. The species specificity of H. assulta females also appeared by the particular large size of two ordinary glomeruli. The accumulating knowledge on how biologically relevant information is encoded in receptor and antennal lobe neurons in heliothines makes these moths particularly interesting for studying the functional organization of the glomeruli. The anatomical atlases of the antennal lobes, as presented here, are prerequisites for identifying glomeruli ascribed to particular functions across sexes and species.
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http://dx.doi.org/10.1002/cne.20692DOI Listing
October 2005

Projections of male-specific receptor neurons in the antennal lobe of the Oriental tobacco budworm moth, Helicoverpa assulta: a unique glomerular organization among related species.

J Comp Neurol 2005 Jun;486(3):209-20

Department of Psychology, Norwegian University of Science and Technology, N-7491 Trondheim, Norway.

The macroglomerular complex in the primary olfactory center of male moths receives information from numerous pheromone-detecting receptor neurons housed in specific sensilla located on the antennae. We investigated the functional organization of the three glomeruli constituting this complex in Helicoverpa assulta, a unique species among heliothine moths as concerns the composition of the pheromone blend. By tip recordings from the male-specific receptor neurons combined with cobalt-lysine stainings, the axon terminals in the brain were traced and subsequently reconstructed by camera lucida drawings. Some were also reconstructed in a digital form. The results showed that the sensilla could be classified into two functional types. A major category housed two colocalized receptor neurons, one responding to the primary pheromone component cis-9-hexadecenal and the other to the behavioral antagonists cis-9-tetradecenal and cis-9-hexadecenol. Cobalt-lysine applied to this sensillum type consistently resulted in two stained axons, each terminating in one of the two large subunits of the macroglomerular complex: the cumulus or the dorsomedial glomerulus. The second, less frequently appearing sensillum type contained a receptor neuron responding to the second pheromone component, cis-11-hexadecenal. Dye applied to this type resulted in stained axon projections in the ventral glomerulus. In an evolutionary context it is particularly interesting that differences of related heliothine species are reflected in the functional organization of the MGC compartments.
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http://dx.doi.org/10.1002/cne.20544DOI Listing
June 2005

Digital atlases of the antennal lobe in two species of tobacco budworm moths, the Oriental Helicoverpa assulta (male) and the American Heliothis virescens (male and female).

J Comp Neurol 2002 Apr;446(2):123-34

Department of Zoology, Norwegian University of Science and Technology, N-7491 Trondheim, Norway.

The antennal lobe of the moth brain is the primary olfactory center processing information about pheromones and plant odors. We present here a digital atlas of the glomerular antennal lobe structures in the male of Helicoverpa assulta and the male and female of Heliothis virescens, based on synaptic antibody staining combined with confocal microscopy. The numbers of the glomeruli in the three specimens were similar, 65, 66, and 62, respectively. Whereas the male antennal lobe has a macroglomerular complex consisting of three and four units in the two species, the female lobe has two enlarged glomeruli at a corresponding position, near the entrance of the antennal nerve. Another large glomerulus, showing homology in the three specimens, is ventrally located. The small size of the heliothine moths is advantageous for confocal microscopy because the entire brain can be visualized as a single image stack. The maps are freely accessible on the internet, and the digital form of the data allows each atlas to be rotated and sectioned at any angle, providing for the identification of glomeruli in different preparations.
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http://dx.doi.org/10.1002/cne.10180DOI Listing
April 2002
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