scholarly journals Distributed representation of social odors indicates parallel processing in the antennal lobe of ants

2011 ◽  
Vol 106 (5) ◽  
pp. 2437-2449 ◽  
Author(s):  
Andreas Simon Brandstaetter ◽  
Christoph Johannes Kleineidam

In colonies of eusocial Hymenoptera cooperation is organized through social odors, and particularly ants rely on a sophisticated odor communication system. Neuronal information about odors is represented in spatial activity patterns in the primary olfactory neuropile of the insect brain, the antennal lobe (AL), which is analog to the vertebrate olfactory bulb. The olfactory system is characterized by neuroanatomical compartmentalization, yet the functional significance of this organization is unclear. Using two-photon calcium imaging, we investigated the neuronal representation of multicomponent colony odors, which the ants assess to discriminate friends (nestmates) from foes (nonnestmates). In the carpenter ant Camponotus floridanus, colony odors elicited spatial activity patterns distributed across different AL compartments. Activity patterns in response to nestmate and nonnestmate colony odors were overlapping. This was expected since both consist of the same components at differing ratios. Colony odors change over time and the nervous system has to constantly adjust for this (template reformation). Measured activity patterns were variable, and variability was higher in response to repeated nestmate than to repeated nonnestmate colony odor stimulation. Variable activity patterns may indicate neuronal plasticity within the olfactory system, which is necessary for template reformation. Our results indicate that information about colony odors is processed in parallel in different neuroanatomical compartments, using the computational power of the whole AL network. Parallel processing might be advantageous, allowing reliable discrimination of highly complex social odors.

2019 ◽  
Author(s):  
S.T. Ferguson ◽  
K.Y. Park ◽  
A. Ruff ◽  
I. Bakis ◽  
L.J. Zwiebel

AbstractBackgroundIn eusocial ants, aggressive behaviors require a sophisticated ability to detect and discriminate between chemical signatures such as cuticular hydrocarbons that distinguish nestmate friends from non-nestmate foes. It has been suggested that a mismatch between a chemical signature (label) and the internal, neuronal representation of the colony odor (template) leads to the recognition of and subsequent aggression between non-nestmates. While several studies have demonstrated that ant chemosensory systems, most notably olfaction, are largely responsible for the decoding of these chemical signatures, a definitive demonstration that odorant receptors are responsible for the detection and processing of the pheromonal signals that regulate nestmate recognition has thus far been lacking. To address this, we have developed an aggression-based bioassay incorporating a suite of highly selective odorant receptor modulators to characterize the role of olfaction in nestmate recognition in the formicine ant Camponotus floridanus.ResultsValidation of our aggression-based behavioral assay was carried out by demonstrating an antennal requirement for nestmate recognition. In order to adapt this bioassay for the volatile delivery of Orco modulators, electroantennography was used to show that both a volatilized Orco antagonist (VUANT1) and an Orco agonist (VUAA4) eliminated or otherwise interfered with the electrophysiological responses to the hydrocarbon decane, respectively. Volatilize administration of these compounds to adult workers significantly reduced aggression between non-nestmates without altering aggression levels between nestmates but did not alter aggressive responses towards a mechanical stimulus.ConclusionsOur studies provide direct evidence that the antennae (as olfactory appendages) and odorant receptors (at the molecular level) are necessary for mediating aggression towards non-nestmates. Furthermore, our observations support a hypothesis in which rejection of non-nestmates depends on the precise detection and decoding of chemical signatures present on non-nestmates as opposed to the absence of any information or the active acceptance of familiar signatures. In addition to describing a novel approach to assess olfactory signaling in genetically intractable insect systems, these studies contribute to a long-standing interest in odor coding and the molecular neuroethology of nestmate recognition.


2005 ◽  
Vol 94 (5) ◽  
pp. 3303-3313 ◽  
Author(s):  
Paul Szyszka ◽  
Mathias Ditzen ◽  
Alexander Galkin ◽  
C. Giovanni Galizia ◽  
Randolf Menzel

We explored the transformations accompanying the transmission of odor information from the first-order processing area, the antennal lobe, to the mushroom body, a higher-order integration center in the insect brain. Using Ca2+ imaging, we recorded activity in the dendrites of the projection neurons that connect the antennal lobe with the mushroom body. Next, we recorded the presynaptic terminals of these projection neurons. Finally, we characterized their postsynaptic partners, the intrinsic neurons of the mushroom body, the clawed Kenyon cells. We found fundamental differences in odor coding between the antennal lobe and the mushroom body. Odors evoked combinatorial activity patterns at all three processing stages, but the spatial patterns became progressively sparser along this path. Projection neuron dendrites and boutons showed similar response profiles, but the boutons were more narrowly tuned to odors. The transmission from projection neuron boutons to Kenyon cells was accompanied by a further sparsening of the population code. Activated Kenyon cells were highly odor specific. Furthermore, the onset of Kenyon cell responses to projection neurons occurred within the first 200 ms and complex temporal patterns were transformed into brief phasic responses. Thus two types of transformations occurred within the MB: sparsening of a combinatorial code, mediated by pre- and postsynaptic processing within the mushroom body microcircuits, and temporal sharpening of postsynaptic Kenyon cell responses, probably involving a broader loop of inhibitory recurrent neurons.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Antoine Couto ◽  
Gérard Arnold ◽  
Hiroyuki Ai ◽  
Jean-Christophe Sandoz

AbstractOlfaction is a crucial sensory modality underlying foraging, social and mating behaviors in many insects. Since the olfactory system is at the interface between the animal and its environment, it receives strong evolutionary pressures that promote neuronal adaptations and phenotypic variations across species. Hornets are large eusocial predatory wasps with a highly developed olfactory system, critical for foraging and intra-specific communication. In their natural range, hornet species display contrasting ecologies and olfactory-based behaviors, which might match to adaptive shifts in their olfactory system. The first olfactory processing center of the insect brain, the antennal lobe, is made of morphological and functional units called glomeruli. Using fluorescent staining, confocal microscopy and 3D reconstructions, we compared antennal lobe structure, glomerular numbers and volumes in four hornet species (Vespa crabro, Vespa velutina, Vespa mandarinia and Vespa orientalis) with marked differences in nesting site preferences and predatory behaviors. Despite a conserved organization of their antennal lobe compartments, glomeruli numbers varied strongly between species, including in a subsystem thought to process intraspecific cuticular signals. Moreover, specific adaptations involving enlarged glomeruli appeared in two species, V. crabro and V. mandarinia, but not in the others. We discuss the possible function of these adaptations based on species-specific behavioral differences.


2010 ◽  
Vol 103 (4) ◽  
pp. 2185-2194 ◽  
Author(s):  
Nina Deisig ◽  
Martin Giurfa ◽  
Jean Christophe Sandoz

Local networks within the primary olfactory centers reformat odor representations from olfactory receptor neurons to second-order neurons. By studying the rules underlying mixture representation at the input to the antennal lobe (AL), the primary olfactory center of the insect brain, we recently found that mixture representation follows a strict elemental rule in honeybees: the more a component activates the AL when presented alone, the more it is represented in a mixture. We now studied mixture representation at the output of the AL by imaging a population of second-order neurons, which convey AL processed odor information to higher brain centers. We systematically measured odor-evoked activity in 22 identified glomeruli in response to four single odorants and all their possible binary, ternary and quaternary mixtures. By comparing input and output responses, we determined how the AL network reformats mixture representation and what advantage this confers for odor discrimination. We show that increased inhibition within the AL leads to more synthetic, less elemental, mixture representation at the output level than that at the input level. As a result, mixture representations become more separable in the olfactory space, thus allowing better differentiation among floral blends in nature.


Author(s):  
Gianluca Serra ◽  
Guido Chelazzi ◽  
Juan C. Castilla

An automated photographic technique was used to collect quantitative information on the activity patterns of Fissurella crassa under heavy-exposed sea conditions.The activity of this key-hole limpet was confined to nocturnal low tides. Total length of excursions was significantly greater during spring tides than neap tides, as was the maximum distance reached from the refuge. Total duration of excursions and their average speed did not vary significantly according to the spring/neap cycle. While the direction angle of excursions relative to the refuge was not influenced significantly by the spring/neap cycle, the lowest zone within the intertidal was reached by F. crassa during spring low tides only.Fissurella crassa showed a spatial activity pattern fluctuating intra/inter-individually between a central place foraging and a ranging strategy, with a marked propensity for the former. Looped excursions were characterized by higher speed for the movements away and toward the limpet's refuge, than the movements at maximum distance from the refuge. As the outward and inward branches of looped excursions often overlapped extensively, trail-following is suggested as the main mechanism of orientation used by F. crassa to relocate the refuge.


2013 ◽  
Vol 109 (2) ◽  
pp. 332-343 ◽  
Author(s):  
Cyrille C. Girardin ◽  
Sabine Kreissl ◽  
C. Giovanni Galizia

The olfactory system is a classical model for studying sensory processing. The first olfactory brain center [the olfactory bulb of vertebrates and the antennal lobe (AL) of insects] contains spherical neuropiles called glomeruli. Each glomerulus receives the information from one olfactory receptor type. Interglomerular computation is accomplished by lateral connectivity via interneurons. However, the spatial and functional organization of these lateral connections is not completely understood. Here we studied the spatial logic in the AL of the honeybee. We combined topical application of neurotransmitters, olfactory stimulations, and in vivo calcium imaging to visualize the arrangement of lateral connections. Suppression of activity in a single glomerulus with γ-aminobutyric acid (GABA) while presenting an odor reveals the existence of inhibitory interactions. Stimulating a glomerulus with acetylcholine (ACh) activates inhibitory interglomerular connections that can reduce odor-evoked responses. We show that this lateral network is patchy, in that individual glomeruli inhibit other glomeruli with graded strength, but in a spatially discontinuous manner. These results suggest that processing of olfactory information requires combinatorial activity patterns with complex topologies across the AL.


2002 ◽  
Vol 162 (2-3) ◽  
pp. 209-218 ◽  
Author(s):  
Michael A. Menzel ◽  
Timothy C. Carter ◽  
Jennifer M. Menzel ◽  
W. Mark Ford ◽  
Brian R. Chapman

Author(s):  
Philipp Schlegel ◽  
Alexander Shakeel Bates ◽  
Tomke Stürner ◽  
Sridhar R. Jagannathan ◽  
Nikolas Drummond ◽  
...  

AbstractThe hemibrain connectome (Scheffer et al., 2020) provides large scale connectivity and morphology information for the majority of the central brain of Drosophila melanogaster. Using this data set, we provide a complete description of the most complex olfactory system studied at synaptic resolution to date, covering all first, second and third-order neurons of the olfactory system associated with the antennal lobe and lateral horn (mushroom body neurons are described in a parallel paper, (Li et al., 2020)). We develop a generally applicable strategy to extract information flow and layered organisation from synaptic resolution connectome graphs, mapping olfactory input to descending interneurons. This identifies a range of motifs including highly lateralised circuits in the antennal lobe and patterns of convergence downstream of the mushroom body and lateral horn. We also leverage a second data set (FAFB, (Zheng et al., 2018)) to provide a first quantitative assessment of inter- versus intra-individual stereotypy. Complete reconstruction of select developmental lineages in two brains (three brain hemispheres) reveals striking similarity in neuronal morphology across brains for >170 cell types. Within and across brains, connectivity correlates with morphology. Notably, neurons of the same morphological type show similar connection variability within one brain as across brains; this property should enable a rigorous quantitative approach to cell typing.


2021 ◽  
Author(s):  
Ettore Tiraboschi ◽  
Luana Leonardelli ◽  
Gianluca Segata ◽  
Elisa Rigosi ◽  
Albrecht Haase

We report that airflow produces a complex activation pattern in the antennal lobes of the honeybee Apis mellifera. Glomerular response maps provide a stereotypical code for the intensity and the dynamics of mechanical stimuli that is superimposed on the olfactory code. We show responses to modulated stimuli suggesting that this combinatorial code could provide information about the intensity, direction, and dynamics of the airflow during flight and waggle dance communication.


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